title: On the importance of balancing selection in plants.
abstract: Balancing selection refers to a variety of selective regimes that maintain advantageous genetic diversity within populations. We review the history of the ideas regarding the types of selection that maintain such polymorphism in flowering plants, notably heterozygote advantage, negative frequency-dependent selection, and spatial heterogeneity. One shared feature of these mechanisms is that whether an allele is beneficial or detrimental is conditional on its frequency in the population. We highlight examples of balancing selection on a variety of discrete traits. These include the well-referenced case of self-incompatibility and recent evidence from species with nuclear-cytoplasmic gynodioecy, both of which exhibit trans-specific polymorphism, a hallmark of balancing selection. We also discuss and give examples of how spatial heterogeneity in particular, which is often thought unlikely to allow protected polymorphism, can maintain genetic variation in plants (which are rooted in place) as a result of microhabitat selection. Lastly, we discuss limitations of the protected polymorphism concept for quantitative traits, where selection can inflate the genetic variance without maintaining specific alleles indefinitely. We conclude that while discrete-morph variation provides the most unambiguous cases of protected polymorphism, they represent only a fraction of the balancing selection at work in plants.
authors: Department of Biology, Indiana University, 1001 East Third Street, Bloomington, IN, 47405, USA.
authors: Lynda F
authors: LF
authors: Delph
authors: Department of Ecology and Evolutionary Biology, University of Kansas, 1200 Sunnyside Avenue, Lawrence, KS, 66045, USA.
authors: John K
authors: JK
authors: Kelly
mesh_terms: D000483:Alleles; D017753:Ecosystem; D005838:Genotype; D006579:Heterozygote; D019684:Magnoliopsida / Q000235:genetics*; D008957:Models, Genetic; D010641:Phenotype; D011110:Polymorphism, Genetic; D012641:Selection, Genetic
keywords: negative frequency-dependent selection; nuclear-cytoplasmic gynodioecy; overdominance; spatial heterogeneity; trans-specific polymorphism
references: Genetics. 2009 Feb;181(2):631-44
references: 19047417
references: Cold Spring Harb Symp Quant Biol. 1955;20:25-31; discussion, 31-2
references: 13433552
references: Genetics. 1939 Jun;24(4):538-52
references: 17246937
references: PLoS Genet. 2012;8(11):e1002992
references: 23133397
references: J Evol Biol. 2013 Mar;26(3):529-44
references: 23286313
references: Genetics. 1976 Sep;84(1):145-57
references: 992363
references: New Phytol. 2013 Dec;200(4):966-77
references: 23952142
references: Evolution. 1984 Jul;38(4):817-832
references: 28555822
references: Nat Rev Genet. 2009 Feb;10(2):83-93
references: 19119264
references: Evolution. 1998 Jun;52(3):678-691
references: 28565238
references: Nat Rev Genet. 2007 Nov;8(11):845-56
references: 17943192
references: Evolution. 1993 Jun;47(3):833-843
references: 28567912
references: Ann Bot. 2012 May;109(6):1125-32
references: 22401850
references: Genetics. 2007 Jul;176(3):1729-40
references: 17483410
references: J Ecol. 2011 Jan;99(1):96-112
references: 21243068
references: J Evol Biol. 2012 Oct;25(10):1918-1936
references: 22905782
references: Evolution. 2004 Nov;58(11):2426-37
references: 15612286
references: Proc Natl Acad Sci U S A. 2002 Sep 3;99(18):11730-5
references: 12192087
references: Genetics. 1989 Jan;121(1):129-38
references: 17246488
references: Science. 2011 Nov 18;334(6058):972-4
references: 22096197
references: Genetics. 1931 Mar;16(2):97-159
references: 17246615
references: Evolution. 1987 Nov;41(6):1290-1301
references: 28563599
references: Nature. 2007 Dec 6;450(7171):870-3
references: 18004303
references: Proc Natl Acad Sci U S A. 2006 Aug 29;103(35):12957-8
references: 16938847
references: Mol Biol Evol. 2009 Nov;26(11):2499-513
references: 19633228
references: PLoS One. 2008;3(12):e4010
references: 19104660
references: Nature. 1999 Aug 12;400(6745):667-71
references: 10458161
references: J Theor Biol. 1978 Jan 20;70(2):213-28
references: 633917
references: Cold Spring Harb Symp Quant Biol. 1955;20:1-15
references: 13433550
references: Mol Biol Evol. 2009 Dec;26(12):2755-64
references: 19713326
references: Curr Biol. 2013 Jul 8;23(13):1256-60
references: 23810533
references: Proc Natl Acad Sci U S A. 2001 May 22;98(11):6253-5
references: 11353863
references: Evolution. 1992 Dec;46(6):1658-1673
references: 28567766
references: Am Nat. 2003 May;161(5):762-76
references: 12858283
references: Mol Ecol. 2004 Oct;13(10):2873-89
references: 15367105
references: Evolution. 1992 Apr;46(2):412-429
references: 28564040
references: Genetics. 1981 Sep;99(1):169-81
references: 17249111
references: Genetics. 2007 Aug;176(4):2465-76
references: 17717197
references: Theor Popul Biol. 1984 Apr;25(2):138-93
references: 6729751
references: Nat Rev Genet. 2009 Nov;10(11):783-96
references: 19834483
references: Am Nat. 2006 Apr;167(4):481-95
references: 16670992
references: Genetics. 2006 Dec;174(4):1983-94
references: 16980398
references: Oecologia. 1995 Jun;102(4):490-493
references: 28306892
references: Proc Natl Acad Sci U S A. 2002 Aug 20;99(17):11525-30
references: 12172007
references: Ann Bot. 2013 Oct;112(6):1169-79
references: 24023042
references: Am Nat. 1998 Jun;151(6):564-9
references: 18811377
references: Science. 2010 Oct 22;330(6003):493-5
references: 20966249
references: Proc R Soc Lond B Biol Sci. 1979 Sep 21;205(1161):453-74
references: 42055
references: Genet Res. 1972 Feb;19(1):17-25
references: 5024710
references: Ecol Lett. 2012 May;15(5):425-35
references: 22372578
references: Naturwissenschaften. 2005 Jun;92(6):255-64
references: 15931514
references: Evolution. 2000 Apr;54(2):691-5
references: 10937244
references: Evolution. 1990 Dec;44(8):2022-2030
references: 28564443
references: Proc Natl Acad Sci U S A. 1990 Dec;87(24):9732-5
references: 2263623
references: Plant Cell. 2006 Aug;18(8):1803-18
references: 16798885
references: Science. 1979 Feb 16;203(4381):658-60
references: 17813380
references: Genetics. 1938 Mar;23(2):190-202
references: 17246880
references: Genetics. 1964 Mar;49(3):411-23
references: 17248201
references: Science. 2011 Apr 1;332(6025):106-9
references: 21454789
references: Genet Res. 2002 Aug;80(1):31-46
references: 12448856
references: Science. 2008 Dec 5;322(5907):1559-62
references: 19056989
references: Heredity (Edinb). 2013 Aug;111(2):157-64
references: 23591518
references: Evolution. 1995 Apr;49(2):241-251
references: 28565006
references: Evolution. 1984 Jul;38(4):796-803
references: 28555829
references: Science. 2001 Jun 22;292(5525):2281-5
references: 11423651
references: Adv Genet. 1997;36:137-55
references: 9348654
references: Oecologia. 2003 Mar;135(1):1-9
references: 12647098
references: Evolution. 2000 Aug;54(4):1173-81
references: 11005286
references: Am J Bot. 2010 Jun;97(6):934-44
references: 21622464