Search tips
Search criteria 


Logo of transbThe Royal Society PublishingPhilosophical Transactions BAboutBrowse By SubjectAlertsFree Trial
Philos Trans R Soc Lond B Biol Sci. 2003 June 29; 358(1434): 1051–1070.
PMCID: PMC1693193

Effects of inbreeding on the genetic diversity of populations.


The study of variability within species is important to all biologists who use genetic markers. Since the discovery of molecular variability among normal individuals, data have been collected from a wide range of organisms, and it is important to understand the major factors affecting diversity levels and patterns. Comparisons of inbreeding and outcrossing populations can contribute to this understanding, and therefore studying plant populations is important, because related species often have different breeding systems. DNA sequence data are now starting to become available from suitable plant and animal populations, to measure and compare variability levels and test predictions.

Full Text

The Full Text of this article is available as a PDF (559K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Aguadé M. Nucleotide sequence variation at two genes of the phenylpropanoid pathway, the FAH1 and F3H genes, in Arabidopsis thaliana. Mol Biol Evol. 2001 Jan;18(1):1–9. [PubMed]
  • Aguade M, Miyashita N, Langley CH. Reduced variation in the yellow-achaete-scute region in natural populations of Drosophila melanogaster. Genetics. 1989 Jul;122(3):607–615. [PubMed]
  • Anderson TJ, Paul RE, Donnelly CA, Day KP. Do malaria parasites mate non-randomly in the mosquito midgut? Genet Res. 2000 Jun;75(3):285–296. [PubMed]
  • Andolfatto P, Nordborg M. The effect of gene conversion on intralocus associations. Genetics. 1998 Mar;148(3):1397–1399. [PubMed]
  • Andolfatto P. Adaptive hitchhiking effects on genome variability. Curr Opin Genet Dev. 2001 Dec;11(6):635–641. [PubMed]
  • Atanassov I, Delichère C, Filatov DA, Charlesworth D, Negrutiu I, Monéger F. Analysis and evolution of two functional Y-linked loci in a plant sex chromosome system. Mol Biol Evol. 2001 Dec;18(12):2162–2168. [PubMed]
  • Baer CF. Among-locus variation in Fst: fish, allozymes and the Lewontin-Krakauer test revisited. Genetics. 1999 Jun;152(2):653–659. [PubMed]
  • BAKER HG. Reproductive methods as factors in speciation in flowering plants. Cold Spring Harb Symp Quant Biol. 1959;24:177–191. [PubMed]
  • Barton N, Bengtsson BO. The barrier to genetic exchange between hybridising populations. Heredity (Edinb) 1986 Dec;57(Pt 3):357–376. [PubMed]
  • Baudry E, Kerdelhué C, Innan H, Stephan W. Species and recombination effects on DNA variability in the tomato genus. Genetics. 2001 Aug;158(4):1725–1735. [PubMed]
  • Begun DJ, Aquadro CF. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature. 1992 Apr 9;356(6369):519–520. [PubMed]
  • Bena G, Prosperi JM, Lejeune B, Olivieri I. Evolution of annual species of the genus Medicago: a molecular phylogenetic approach. Mol Phylogenet Evol. 1998 Jun;9(3):552–559. [PubMed]
  • Bergelson J, Stahl E, Dudek S, Kreitman M. Genetic variation within and among populations of Arabidopsis thaliana. Genetics. 1998 Mar;148(3):1311–1323. [PubMed]
  • Bergelson J, Kreitman M, Stahl EA, Tian D. Evolutionary dynamics of plant R-genes. Science. 2001 Jun 22;292(5525):2281–2285. [PubMed]
  • Birky CW, Jr, Maruyama T, Fuerst P. An approach to population and evolutionary genetic theory for genes in mitochondria and chloroplasts, and some results. Genetics. 1983 Mar;103(3):513–527. [PubMed]
  • Bousquet J, Strauss SH, Doerksen AH, Price RA. Extensive variation in evolutionary rate of rbcL gene sequences among seed plants. Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7844–7848. [PubMed]
  • Braverman JM, Hudson RR, Kaplan NL, Langley CH, Stephan W. The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics. 1995 Jun;140(2):783–796. [PubMed]
  • Brown AH, Feldman MW, Nevo E. Multilocus Structure of Natural Populations of HORDEUM SPONTANEUM. Genetics. 1980 Oct;96(2):523–536. [PubMed]
  • Bustamante Carlos D, Nielsen Rasmus, Sawyer Stanley A, Olsen Kenneth M, Purugganan Michael D, Hartl Daniel L. The cost of inbreeding in Arabidopsis. Nature. 2002 Apr 4;416(6880):531–534. [PubMed]
  • Charlesworth B. Measures of divergence between populations and the effect of forces that reduce variability. Mol Biol Evol. 1998 May;15(5):538–543. [PubMed]
  • Charlesworth B, Morgan MT, Charlesworth D. The effect of deleterious mutations on neutral molecular variation. Genetics. 1993 Aug;134(4):1289–1303. [PubMed]
  • Charlesworth B, Nordborg M, Charlesworth D. The effects of local selection, balanced polymorphism and background selection on equilibrium patterns of genetic diversity in subdivided populations. Genet Res. 1997 Oct;70(2):155–174. [PubMed]
  • Charlesworth D, Awadalla P. Flowering plant self-incompatibility: the molecular population genetics of Brassica S-loci. Heredity (Edinb) 1998 Jul;81(Pt 1):1–9. [PubMed]
  • Charlesworth D, Yang Z. Allozyme diversity in Leavenworthia populations with different inbreeding levels. Heredity (Edinb) 1998 Oct;81(Pt 4):453–461. [PubMed]
  • Charlesworth D, Charlesworth B, Strobeck C. Selection for recombination in partially self-fertilizing populations. Genetics. 1979 Sep;93(1):237–244. [PubMed]
  • Charlesworth D, Charlesworth B, Morgan MT. The pattern of neutral molecular variation under the background selection model. Genetics. 1995 Dec;141(4):1619–1632. [PubMed]
  • Copenhaver GP, Nickel K, Kuromori T, Benito MI, Kaul S, Lin X, Bevan M, Murphy G, Harris B, Parnell LD, et al. Genetic definition and sequence analysis of Arabidopsis centromeres. Science. 1999 Dec 24;286(5449):2468–2474. [PubMed]
  • Cummings MP, Clegg MT. Nucleotide sequence diversity at the alcohol dehydrogenase 1 locus in wild barley (Hordeum vulgare ssp. spontaneum): an evaluation of the background selection hypothesis. Proc Natl Acad Sci U S A. 1998 May 12;95(10):5637–5642. [PubMed]
  • Currat Mathias, Trabuchet Guy, Rees David, Perrin Pascale, Harding Rosalind M, Clegg John B, Langaney André, Excoffier Laurent. Molecular analysis of the beta-globin gene cluster in the Niokholo Mandenka population reveals a recent origin of the beta(S) Senegal mutation. Am J Hum Genet. 2002 Jan;70(1):207–223. [PubMed]
  • Dvornyk Volodymyr, Sirviö Anu, Mikkonen Merja, Savolainen Outi. Low nucleotide diversity at the pal1 locus in the widely distributed Pinus sylvestris. Mol Biol Evol. 2002 Feb;19(2):179–188. [PubMed]
  • Eyre-Walker A, Gaut BS. Correlated rates of synonymous site evolution across plant genomes. Mol Biol Evol. 1997 Apr;14(4):455–460. [PubMed]
  • Eyre-Walker A, Gaut RL, Hilton H, Feldman DL, Gaut BS. Investigation of the bottleneck leading to the domestication of maize. Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4441–4446. [PubMed]
  • Fay JC, Wu CI. A human population bottleneck can account for the discordance between patterns of mitochondrial versus nuclear DNA variation. Mol Biol Evol. 1999 Jul;16(7):1003–1005. [PubMed]
  • Fay JC, Wyckoff GJ, Wu CI. Positive and negative selection on the human genome. Genetics. 2001 Jul;158(3):1227–1234. [PubMed]
  • Fay Justin C, Wyckoff Gerald J, Wu Chung-I. Testing the neutral theory of molecular evolution with genomic data from Drosophila. Nature. 2002 Feb 28;415(6875):1024–1026. [PubMed]
  • Filatov DA, Charlesworth D. DNA polymorphism, haplotype structure and balancing selection in the Leavenworthia PgiC locus. Genetics. 1999 Nov;153(3):1423–1434. [PubMed]
  • Filatov DA, Monéger F, Negrutiu I, Charlesworth D. Low variability in a Y-linked plant gene and its implications for Y-chromosome evolution. Nature. 2000 Mar 23;404(6776):388–390. [PubMed]
  • Filatov DA, Laporte V, Vitte C, Charlesworth D. DNA diversity in sex-linked and autosomal genes of the plant species Silene latifolia and Silene dioica. Mol Biol Evol. 2001 Aug;18(8):1442–1454. [PubMed]
  • Fu YX, Li WH. Statistical tests of neutrality of mutations. Genetics. 1993 Mar;133(3):693–709. [PubMed]
  • Fullerton SM, Harding RM, Boyce AJ, Clegg JB. Molecular and population genetic analysis of allelic sequence diversity at the human beta-globin locus. Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1805–1809. [PubMed]
  • Galtier N, Depaulis F, Barton NH. Detecting bottlenecks and selective sweeps from DNA sequence polymorphism. Genetics. 2000 Jun;155(2):981–987. [PubMed]
  • Gitzendanner MA, Soltis PS. Patterns of genetic variation in rare and widespread plant congeners. Am J Bot. 2000 Jun;87(6):783–792. [PubMed]
  • Graustein Andrew, Gaspar John M, Walters James R, Palopoli Michael F. Levels of DNA polymorphism vary with mating system in the nematode genus caenorhabditis. Genetics. 2002 May;161(1):99–107. [PubMed]
  • Hagenblad Jenny, Nordborg Magnus. Sequence variation and haplotype structure surrounding the flowering time locus FRI in Arabidopsis thaliana. Genetics. 2002 May;161(1):289–298. [PubMed]
  • Hedrick PW. Hitchhiking: a comparison of linkage and partial selfing. Genetics. 1980 Mar;94(3):791–808. [PubMed]
  • Hinata K, Watanabe M, Yamakawa S, Satta Y, Isogai A. Evolutionary aspects of the S-related genes of the Brassica self-incompatibility system: synonymous and nonsynonymous base substitutions. Genetics. 1995 Jul;140(3):1099–1104. [PubMed]
  • Hudson RR, Kaplan NL. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics. 1985 Sep;111(1):147–164. [PubMed]
  • Hudson RR, Kreitman M, Aguadé M. A test of neutral molecular evolution based on nucleotide data. Genetics. 1987 May;116(1):153–159. [PubMed]
  • Hudson RR, Boos DD, Kaplan NL. A statistical test for detecting geographic subdivision. Mol Biol Evol. 1992 Jan;9(1):138–151. [PubMed]
  • Hudson RR, Sáez AG, Ayala FJ. DNA variation at the Sod locus of Drosophila melanogaster: an unfolding story of natural selection. Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):7725–7729. [PubMed]
  • Ingvarsson Pär K. A metapopulation perspective on genetic diversity and differentiation in partially self-fertilizing plants. Evolution. 2002 Dec;56(12):2368–2373. [PubMed]
  • Innan Hideki, Tajima Fumio. A statistical test for the difference in the amounts of DNA variation between two populations. Genet Res. 2002 Aug;80(1):15–25. [PubMed]
  • Kaplan NL, Hudson RR, Langley CH. The "hitchhiking effect" revisited. Genetics. 1989 Dec;123(4):887–899. [PubMed]
  • Kawabe A, Yamane K, Miyashita NT. DNA polymorphism at the cytosolic phosphoglucose isomerase (PgiC) locus of the wild plant Arabidopsis thaliana. Genetics. 2000 Nov;156(3):1339–1347. [PubMed]
  • Koch MA, Weisshaar B, Kroymann J, Haubold B, Mitchell-Olds T. Comparative genomics and regulatory evolution: conservation and function of the Chs and Apetala3 promoters. Mol Biol Evol. 2001 Oct;18(10):1882–1891. [PubMed]
  • Koch R, van Luenen HG, van der Horst M, Thijssen KL, Plasterk RH. Single nucleotide polymorphisms in wild isolates of Caenorhabditis elegans. Genome Res. 2000 Nov;10(11):1690–1696. [PubMed]
  • Kondo Katsuhiko, Yamamoto Mayu, Itahashi Ryoko, Sato Takanori, Egashira Hiroaki, Hattori Tsukaho, Kowyama Yasuo. Insights into the evolution of self-compatibility in Lycopersicon from a study of stylar factors. Plant J. 2002 Apr;30(2):143–153. [PubMed]
  • Kraft T, Säll T, Magnusson-Rading I, Nilsson NO, Halldén C. Positive correlation between recombination rates and levels of genetic variation in natural populations of sea beet (Beta vulgaris subsp. maritima). Genetics. 1998 Nov;150(3):1239–1244. [PubMed]
  • Krauss SL. Accurate gene diversity estimates from amplified fragment length polymorphism (AFLP) markers. Mol Ecol. 2000 Sep;9(9):1241–1245. [PubMed]
  • Kreitman M. Methods to detect selection in populations with applications to the human. Annu Rev Genomics Hum Genet. 2000;1:539–559. [PubMed]
  • Laporte Valérie, Charlesworth Brian. Effective population size and population subdivision in demographically structured populations. Genetics. 2002 Sep;162(1):501–519. [PubMed]
  • Le Corre Valérie, Roux Fabrice, Reboud Xavier. DNA polymorphism at the FRIGIDA gene in Arabidopsis thaliana: extensive nonsynonymous variation is consistent with local selection for flowering time. Mol Biol Evol. 2002 Aug;19(8):1261–1271. [PubMed]
  • Lewontin RC, Krakauer J. Distribution of gene frequency as a test of the theory of the selective neutrality of polymorphisms. Genetics. 1973 May;74(1):175–195. [PubMed]
  • Lin Jing-Zhong, Morrell Peter L, Clegg Michael T. The influence of linkage and inbreeding on patterns of nucleotide sequence diversity at duplicate alcohol dehydrogenase loci in wild barley (Hordeum vulgare ssp. spontaneum). Genetics. 2002 Dec;162(4):2007–2015. [PubMed]
  • Liu F, Zhang L, Charlesworth D. Genetic diversity in Leavenworthia populations with different inbreeding levels. Proc Biol Sci. 1998 Feb 22;265(1393):293–301. [PMC free article] [PubMed]
  • Luikart G, Allendorf FW, Cornuet JM, Sherwin WB. Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered. 1998 May-Jun;89(3):238–247. [PubMed]
  • Lynch M, O'Hely M, Walsh B, Force A. The probability of preservation of a newly arisen gene duplicate. Genetics. 2001 Dec;159(4):1789–1804. [PubMed]
  • McCauley DE. Contrasting the distribution of chloroplast DNA and allozyme polymorphism among local populations of Silene alba: implications for studies of gene flow in plants. Proc Natl Acad Sci U S A. 1994 Aug 16;91(17):8127–8131. [PubMed]
  • Martin FW. The Genetic Control of Unilateral Incompatibility between Two Tomato Species. Genetics. 1967 Jul;56(3):391–398. [PubMed]
  • Maruyama T, Birky CW., Jr Effects of periodic selection on gene diversity in organelle genomes and other systems without recombination. Genetics. 1991 Feb;127(2):449–451. [PubMed]
  • Miyashita NT, Aguadé M, Langley CH. Linkage disequilibrium in the white locus region of Drosophila melanogaster. Genet Res. 1993 Oct;62(2):101–109. [PubMed]
  • Mougel Christophe, Thioulouse Jean, Perrière Guy, Nesme Xavier. A mathematical method for determining genome divergence and species delineation using AFLP. Int J Syst Evol Microbiol. 2002 Mar;52(Pt 2):573–586. [PubMed]
  • Nagylaki T. Fixation indices in subdivided populations. Genetics. 1998 Mar;148(3):1325–1332. [PubMed]
  • Nagylaki T. Geographical invariance and the strong-migration limit in subdivided populations. J Math Biol. 2000 Aug;41(2):123–142. [PubMed]
  • Nasrallah JB, Nasrallah ME. The molecular genetics of self-incompatibility in Brassica. Annu Rev Genet. 1989;23:121–139. [PubMed]
  • Navarro Arcadio, Barton Nick H. The effects of multilocus balancing selection on neutral variability. Genetics. 2002 Jun;161(2):849–863. [PubMed]
  • Newton AC, Allnutt TR, Gillies AC, Lowe AJ, Ennos RA. Molecular phylogeography, intraspecific variation and the conservation of tree species. Trends Ecol Evol. 1999 Apr;14(4):140–145. [PubMed]
  • Nordborg M. Structured coalescent processes on different time scales. Genetics. 1997 Aug;146(4):1501–1514. [PubMed]
  • Nordborg M. Linkage disequilibrium, gene trees and selfing: an ancestral recombination graph with partial self-fertilization. Genetics. 2000 Feb;154(2):923–929. [PubMed]
  • Nordborg M, Donnelly P. The coalescent process with selfing. Genetics. 1997 Jul;146(3):1185–1195. [PubMed]
  • Nordborg Magnus, Innan Hideki. Molecular population genetics. Curr Opin Plant Biol. 2002 Feb;5(1):69–73. [PubMed]
  • Nordborg Magnus, Innan Hideki. The genealogy of sequences containing multiple sites subject to strong selection in a subdivided population. Genetics. 2003 Mar;163(3):1201–1213. [PubMed]
  • Nordborg Magnus, Borevitz Justin O, Bergelson Joy, Berry Charles C, Chory Joanne, Hagenblad Jenny, Kreitman Martin, Maloof Julin N, Noyes Tina, Oefner Peter J, et al. The extent of linkage disequilibrium in Arabidopsis thaliana. Nat Genet. 2002 Feb;30(2):190–193. [PubMed]
  • Pannell JR, Charlesworth B. Effects of metapopulation processes on measures of genetic diversity. Philos Trans R Soc Lond B Biol Sci. 2000 Dec 29;355(1404):1851–1864. [PMC free article] [PubMed]
  • Pollak E. On the theory of partially inbreeding finite populations. I. Partial selfing. Genetics. 1987 Oct;117(2):353–360. [PubMed]
  • Pritchard JK, Przeworski M. Linkage disequilibrium in humans: models and data. Am J Hum Genet. 2001 Jul;69(1):1–14. [PubMed]
  • Przeworski M, Wall JD. Why is there so little intragenic linkage disequilibrium in humans? Genet Res. 2001 Apr;77(2):143–151. [PubMed]
  • Purugganan MD, Boyles AL, Suddith JI. Variation and selection at the CAULIFLOWER floral homeotic gene accompanying the evolution of domesticated Brassica oleracea. Genetics. 2000 Jun;155(2):855–862. [PubMed]
  • Richman AD, Uyenoyama MK, Kohn JR. Allelic diversity and gene genealogy at the self-incompatibility locus in the Solanaceae. Science. 1996 Aug 30;273(5279):1212–1216. [PubMed]
  • Richman AD, Uyenoyama MK, Kohn JR. S-allele diversity in a natural population of Physalis crassifolia (Solanaceae) (ground cherry) assessed by RT-PCR. Heredity (Edinb) 1996 May;76(Pt 5):497–505. [PubMed]
  • Savolainen O, Langley CH, Lazzaro BP, Fr H. Contrasting patterns of nucleotide polymorphism at the alcohol dehydrogenase locus in the outcrossing Arabidopsis lyrata and the selfing Arabidopsis thaliana. Mol Biol Evol. 2000 Apr;17(4):645–655. [PubMed]
  • Schierup MH, Charlesworth D, Vekemans X. The effect of hitch-hiking on genes linked to a balanced polymorphism in a subdivided population. Genet Res. 2000 Aug;76(1):63–73. [PubMed]
  • Schierup MH, Vekemans X, Charlesworth D. The effect of subdivision on variation at multi-allelic loci under balancing selection. Genet Res. 2000 Aug;76(1):51–62. [PubMed]
  • Schierup MH, Mable BK, Awadalla P, Charlesworth D. Identification and characterization of a polymorphic receptor kinase gene linked to the self-incompatibility locus of Arabidopsis lyrata. Genetics. 2001 May;158(1):387–399. [PubMed]
  • Schoen DJ, Brown AH. Intraspecific variation in population gene diversity and effective population size correlates with the mating system in plants. Proc Natl Acad Sci U S A. 1991 May 15;88(10):4494–4497. [PubMed]
  • Sharbel TF, Haubold B, Mitchell-Olds T. Genetic isolation by distance in Arabidopsis thaliana: biogeography and postglacial colonization of Europe. Mol Ecol. 2000 Dec;9(12):2109–2118. [PubMed]
  • Shiba Hiroshi, Iwano Megumi, Entani Tetsuyuki, Ishimoto Kyoko, Shimosato Hiroko, Che Fang-Sik, Satta Yoko, Ito Akiko, Takada Yoshinobu, Watanabe Masao, et al. The dominance of alleles controlling self-incompatibility in Brassica pollen is regulated at the RNA level. Plant Cell. 2002 Feb;14(2):491–504. [PubMed]
  • Slatkin M. Gene flow and genetic drift in a species subject to frequent local extinctions. Theor Popul Biol. 1977 Dec;12(3):253–262. [PubMed]
  • Slatkin M. The average number of sites separating DNA sequences drawn from a subdivided population. Theor Popul Biol. 1987 Aug;32(1):42–49. [PubMed]
  • Slatkin M. Linkage disequilibrium in growing and stable populations. Genetics. 1994 May;137(1):331–336. [PubMed]
  • Slatkin M, Wiehe T. Genetic hitch-hiking in a subdivided population. Genet Res. 1998 Apr;71(2):155–160. [PubMed]
  • Steinbachs JE, Holsinger KE. S-RNase-mediated gametophytic self-incompatibility is ancestral in eudicots. Mol Biol Evol. 2002 Jun;19(6):825–829. [PubMed]
  • Stephan W, Langley CH. DNA polymorphism in lycopersicon and crossing-over per physical length. Genetics. 1998 Dec;150(4):1585–1593. [PubMed]
  • Strobeck C. Heterozygosity in pin-thrum plants or with partial sex linkage. Genetics. 1972 Dec;72(4):667–678. [PubMed]
  • Strobeck C. Average number of nucleotide differences in a sample from a single subpopulation: a test for population subdivision. Genetics. 1987 Sep;117(1):149–153. [PubMed]
  • Tajima F. The effect of change in population size on DNA polymorphism. Genetics. 1989 Nov;123(3):597–601. [PubMed]
  • Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989 Nov;123(3):585–595. [PubMed]
  • Takahata N. A simple genealogical structure of strongly balanced allelic lines and trans-species evolution of polymorphism. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2419–2423. [PubMed]
  • Takahata N, Satta Y. Footprints of intragenic recombination at HLA loci. Immunogenetics. 1998 May;47(6):430–441. [PubMed]
  • Takebayashi N, Morrell PL. Is self-fertilization an evolutionary dead end? Revisiting an old hypothesis with genetic theories and a macroevolutionary approach. Am J Bot. 2001 Jul;88(7):1143–1150. [PubMed]
  • Tenaillon MI, Sawkins MC, Long AD, Gaut RL, Doebley JF, Gaut BS. Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L.). Proc Natl Acad Sci U S A. 2001 Jul 31;98(16):9161–9166. [PubMed]
  • Terachi T, Yamaguchi K, Yamagishi H. Sequence analysis on the mitochondrial orfB locus in normal and Ogura male-sterile cytoplasms from wild and cultivated radishes. Curr Genet. 2001 Dec;40(4):276–281. [PubMed]
  • Tiffin Peter, Hahn Matthew W. Coding sequence divergence between two closely related plant species: Arabidopsis thaliana and Brassica rapa ssp. pekinensis. J Mol Evol. 2002 Jun;54(6):746–753. [PubMed]
  • Tishkoff SA, Dietzsch E, Speed W, Pakstis AJ, Kidd JR, Cheung K, Bonné-Tamir B, Santachiara-Benerecetti AS, Moral P, Krings M. Global patterns of linkage disequilibrium at the CD4 locus and modern human origins. Science. 1996 Mar 8;271(5254):1380–1387. [PubMed]
  • Uyenoyama MK. A generalized least-squares estimate for the origin of sporophytic self-incompatibility. Genetics. 1995 Feb;139(2):975–992. [PubMed]
  • van Treuren R, Kuittinen H, Kärkkäinen K, Baena-Gonzalez E, Savolainen O. Evolution of microsatellites in Arabis petraea and Arabis lyrata, outcrossing relatives of Arabidopsis thaliana. Mol Biol Evol. 1997 Mar;14(3):220–229. [PubMed]
  • Vekemans X, Slatkin M. Gene and allelic genealogies at a gametophytic self-incompatibility locus. Genetics. 1994 Aug;137(4):1157–1165. [PubMed]
  • Volis Sergei, Mendlinger Samuel, Turuspekov Yerlan, Esnazarov Usken. Phenotypic and allozyme variation in Mediterranean and desert populations of wild barley, Hordeum spontaneum Koch. Evolution. 2002 Jul;56(7):1403–1415. [PubMed]
  • Volkman SK, Barry AE, Lyons EJ, Nielsen KM, Thomas SM, Choi M, Thakore SS, Day KP, Wirth DF, Hartl DL. Recent origin of Plasmodium falciparum from a single progenitor. Science. 2001 Jul 20;293(5529):482–484. [PubMed]
  • Wakeley J. The variance of pairwise nucleotide differences in two populations with migration. Theor Popul Biol. 1996 Feb;49(1):39–57. [PubMed]
  • Wakeley J. The effects of subdivision on the genetic divergence of populations and species. Evolution. 2000 Aug;54(4):1092–1101. [PubMed]
  • Wakeley J, Aliacar N. Gene genealogies in a metapopulation. Genetics. 2001 Oct;159(2):893–905. [PubMed]
  • Wang RL, Stec A, Hey J, Lukens L, Doebley J. The limits of selection during maize domestication. Nature. 1999 Mar 18;398(6724):236–239. [PubMed]
  • Whitlock MC, Barton NH. The effective size of a subdivided population. Genetics. 1997 May;146(1):427–441. [PubMed]
  • Whitlock MC, McCauley DE. Indirect measures of gene flow and migration: FST not equal to 1/(4Nm + 1). Heredity (Edinb) 1999 Feb;82(Pt 2):117–125. [PubMed]
  • Wolfe KH, Li WH, Sharp PM. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci U S A. 1987 Dec;84(24):9054–9058. [PubMed]
  • Wright S. The Distribution of Self-Sterility Alleles in Populations. Genetics. 1939 Jun;24(4):538–552. [PubMed]
  • Wright Stephen I, Lauga Beatrice, Charlesworth Deborah. Rates and patterns of molecular evolution in inbred and outbred Arabidopsis. Mol Biol Evol. 2002 Sep;19(9):1407–1420. [PubMed]

Articles from Philosophical Transactions of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society