Wills, Christopher. Rapid recent human evolution and the acccumulation of balanced genetic polymorphisms. High Alt. Med. Biol. 12:149–155, 2011.—All evolutionary change can be traced to alterations in allele frequencies in populations over time. DNA sequencing on a massive scale now permits us to follow the genetic consequences as our species has diverged from our close relatives and as we have colonized different parts of the world and adapted to them. But it has been difficult to disentangle natural selection from many other factors that alter frequencies. These factors include mutation and intragenic reciprocal recombination, gene conversion, segregation distortion, random drift, and gene flow between populations (these last two are greatly influenced by splits and coalescences of populations over time).
The first part of this review examines recent studies that have had some success in dissecting out the role of natural selection, especially in humans and Drosophila. Among many examples, these studies include those that have followed the rapid evolution of traits that may permit adaptation to high altitude in Tibetan and Andean populations. In some cases, directional selection has been so strong that it may have swept alleles close to fixation in the span of a few thousand years, a rapidity of change that is also sometimes encountered in other organisms.
The second part of the review summarizes data showing that remarkably few alleles have been carried completely to fixation during our recent evolution. Some of the alleles that have not reached fixation may be approaching new internal equilibria, which would indicate polymorphisms that are maintained by balancing selection. Finally, the review briefly examines why genetic polymorphisms, particularly those that are maintained by negative frequency dependence, are likely to have played an important role in the evolution of our species. A method is suggested for measuring the contribution of these polymorphisms to our gene pool. Such polymorphisms may add to the ability of our species to adapt to our increasingly complex and challenging environment.
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References
1.
AguadeM., MiyashitaN., LangleyC.H.1988. Reduced variation in the yellow-achaete-scute region in natural populationsof Drosophila melanogaster. Genetics., 122:607–615.
2.
AidooM., TerlouwD.J., KolczakM., McElroyP.D., ter KuileF.O., KariukiS., NahlenB.L., LalA.A., UdhayakumarV.2002. Protective effects of the sickle cell gene against malaria morbidity and mortality. Lancet., 359:1311–1312.
3.
Alfonso-SanchezM.A., Perez-MirandaA.M., Garcia-ObregonS., PenaJ.A.2010. An evolutionary approach to the high frequency of the Delta F508 CFTR mutation in European populations. Med. Hypotheses., 74:989–992.
4.
AndolfattoP.2005. Adaptive evolution of non-coding DNA in Drosophila. Nature., 437:1149–1152.
5.
BeallC.M., CavalleriG.L., DengL., ElstonR.C., GaoY., KnightJ., LiC., LiJ.C., LiangY., McCormackM.et al.2010. Natural selection on EPAS1 (HIF2) associated with low hemoglobin concentration in Tibetan highlanders. Proc. Natl. Acad. Sci., 107:11459–11464.
6.
BeharD.M., VillemsR., SoodyallH., Blue-SmithJ., PereiraL., MetspaluE., ScozzariR., MakkanH., TzurS., ComasD.et al.2008. The dawn of human matrilineal diversity. Am. J. Hum. Genetics, 82:1130–1140.
7.
Beja-PereiraA., LuikartG., EnglandP.R., BradleyD.G., JannO.C., BertorelleG., ChamberlainA.T., NunesT.P., MetodievS., FerrandN.et al.2003. Gene-culture coevolution between cattle milk protein genes and human lactase genes. Nat. Genetics., 35:311–313.
8.
Berniell-LeeG., CalafellF., BoschE., HeyerE., SicaL., Mouguiama-DaoudaP., van der VeenL., HombertJ.M., Quintana-MurciL., ComasD.2009. Genetic and demographic implications of the Bantu expansion: insights from human paternal lineages. Mol. Biol. Evolution., 26:1581–1589.
9.
BersaglieriT., SabetiP.C., PattersonN., VanderploegT., SchaffnerS.F., DrakeJ.A., RhodesM., ReichD.E., HirschhornJ.N.2004. Genetic signatures of strong recent positive selection at the lactase gene. Am. J. Hum. Genetics., 74:1111–1120.
10.
BighamA., BauchetM., PintoD., MaoX., AkeyJ.M., MeiR., SchererS.W., JulianC.G., WilsonM.J., López HerrézD.et al.2010. Identifying signatures of natural selection in Tibetan and Andean populations using dense genome scan data. PLoS Genet, 6:e1001116.
11.
BighamA.W., MaoX., MeiR., BrutsaertT., WilsonM.J., JulianC.G., ParraE.J., AkeyJ.M., MooreL.G., ShriverM.D.2009. Identifying positive selection candidate loci for high-altitude adaptation in Andean populations. Hum. Genomics., 4:79–90.
12.
BorghansJ.A.M., BeltmanJ.B., De BoerR.J.2004. MHC polymorphism under host–pathogen coevolution. Immunogenetics., 55:732–739.
13.
CoopG., PickrellJ.K., NovembreJ., KudaravalliS., LiJ., AbsherD., MyersR.M., Cavalli-SforzaL.L., FeldmanM.W., PritchardJ.K.2009. The role of geography in human adaptation. PLoS Genet, 5:e1000500.
14.
DumontB.L., PayseurB.A.2008. Evolution of the genomic rate of recombination in mammals. Evolution., 62:276–294.
15.
EhrmanL.1970. The mating advantage of rare males in Drosophila. Proc. Natl. Acad. Sci. U.S.A., 65:345–348.
16.
Eyre-WalkerA., KeightleyP.D.1999. High genomic deleterious mutation rates in hominids. Nature., 397:344–347.
17.
FayJ.C., WyckoffG.J., WuC.I.2002. Testing the neutral theory of molecular evolution with genomic data from Drosophila. Nature., 415:1024–1026.
18.
FazzariM.J., GreallyJ.M.2010. Introduction to epigenomics and epigenome-wide analysis. Methods. Mol. Biol., 620:243–265.
19.
GardnerH.1993. Multiple Intelligences: The Theory in Practice. Basic Books: New York.
20.
HalleggerM., LlorianM., SmithC.W.2010. Alternative splicing: global insights. FEBS J., 277:856–866.
21.
HartlD.2000. A Primer of Population Genetics. Sinauer: Sunderland, MA.
22.
HawksJ., WangE.T., CochranG.M., HarpendingH.C., MoyzisR.K.2007. Recent acceleration of human adaptive evolution. Proc. Natl. Acad. Sci., 104:20753–20758.
23.
HudsonR.R., KreitmanM., AguadeM.1987. A test of neutral molecular evolution based on nucleotide data. Genetics., 116:153–159.
24.
IngmanM., KaessmannH., PaaboS., GyllenstenU.2000. Mitochondrial genome variation and the origin of modern humans. Nature., 408:708–713.
25.
JohnsonW.E., SawyerS.L.2009. Molecular evolution of the antiretroviral TRIM5 gene. Immunogenetics., 61:163–176.
26.
JonesJ.S.1994. The Language of Genes: Solving the Mysteries of Our Genetic Past, Present and Future. Doubleday: New York.
27.
KaplanN.L., HudsonR.R., LangleyC.H.1989. The “hitch-hiking effect” revisited. Genetics., 123:887–899.
28.
KimuraM., OhtaT.1974. On some principles governing molecular evolution. Proc. Natl. Acad. Sci. USA., 71:2848–2852.
29.
KleinJ., SatoA., NikolaidisN.2007. MHC, TSP, and the origin of species: from immunogenetics to evolutionary genetics. Annu. Rev. Genetics., 41:281–304.
30.
KreitmanM.1983. Nucleotide polymorphism at the alcohol dehydrogenase locus of Drosophila melanogaster. Nature., 304:412–417.
31.
KryukovG.V., PennacchioL.A., SunyaevS.R.2007. Most rare missense alleles are deleterious in humans: implications for complex disease and association studies. Am. J. Hum. Genetics., 80:727–739.
LindbergJ., LundebergJ.2010. The plasticity of the mammalian transcriptome. Genomics., 95:1–6.
34.
LiuQ., ParooZ.2010. Biochemical principles of small RNA pathways. Annu. Rev. Biochem., 79:295–319.
35.
López HerrézD., BauchetM., TangK., TheunertC., PugachI., LiJ., NandineniM.R., GrossA., ScholzM., StonekingM.et al.2009. Genetic variation and recent positive selection in worldwide human populations: evidence from nearly 1 million SNPs. PLoS ONE, 4:e7888.
36.
MaherB.2008. Personal genomes: the case of the missing heritability. Nature., 456:18–21.
37.
MazessR.B.1965. Neonatal mortality and altitude in Peru. Am. J. Phys. Anthropol., 23:209–213.
38.
McDonaldJ.H., KreitmanM.1991. Adaptive protein evolution at the Adh locus in Drosophila. Nature., 351:652–654.
39.
MessierW., StewartC.-B.1997. Episodic adaptive evolution of primate lysozymes. Nature., 385:151–154.
40.
NielsenR.2001. Statistical tests of selective neutrality in the age of genomics. Heredity., 86:641–647.
41.
NielsenR., HellmannI., HubiszM., BustamanteC., ClarkA.G.2007. Recent and ongoing selection in the human genome. Nat. Rev. Genetics., 8:857–868.
42.
NortonH.L., KittlesR.A., ParraE., McKeigueP., MaoX., ChengK., CanfieldV.A., BradleyD.G., McEvoyB., ShriverM.D.2007. Genetic evidence for the convergent evolution of light skin in Europeans and East Asians. Mol. Biol. Evolution., 24:710–722.
43.
OhnoS.1972. So much "junk" DNA in our genome. Brookhaven Symp. Biol., 23:366–370.
44.
PickrellJ.K., CoopG., NovembreJ., KudaravalliS., LiJ.Z., AbsherD., SrinivasanB.S., BarshG.S., MyersR.M., FeldmanM.W.et al.2009. Signals of recent positive selection in a worldwide sample of human populations. Genome Res., 19:826–837.
45.
RichardsM.2003. The Neolithic invasion of Europe. Annu. Rev. Anthropol., 32:135–162.
46.
SabetiP.C.2006. Positive natural selection in the human lineage. Science., 312:1614–1620.
47.
SchoenfelderS., ClayI., FraserP.2010. The transcriptional interactome: gene expression in 3D. Curr. Opinion Genetics Dev., 20:127–133.
48.
SellaG., PetrovD.A., PrzeworskiM., AndolfattoP.2009. Pervasive natural selection in the Drosophila genome?PLoS Genetics, 5:e1000495.
49.
ShiH., ZhongH., PengY., DongY.-L., QiX.-B., ZhangF., LiuL.-F., TanS.-J., MaR.Z., XiaoC.-J.et al.2008. Y chromosome evidence of earliest modern human settlement in East Asia and multiple origins of Tibetan and Japanese populations. BMC Biology 6, Article No., 45.
50.
SimonsonT.S., YangY., HuffC.D., YunH., QinG., WitherspoonD.J., BaiZ., LorenzoF.R., XingJ., JordeL.B.et al.2010. Genetic evidence for high-altitude adaptation in Tibet. Science., 329:72–75.
51.
TajimaF.1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics., 123:585–595.
52.
Thousand Genome Consortium. 2010. A map of human genome variation from population-scale sequencing. Nature., 467:1061–1073.
53.
TishkoffS.A., ReedF.A., RanciaroA., VoightB.F., BabbittC.C., SilvermanJ.S., PowellK., MortensenH.M., HirboJ.B., OsmanM.et al.2007. Convergent adaptation of human lactase persistence in Africa and Europe. Nat. Genetics., 39:31–40.
54.
WardP.2001. Future Evolution. Henry Holt: New York.
55.
WillsC.1998. Children of Prometheus: the Accelerating Pace of Human Evolution. Perseus Books, Reading: MA.
56.
XueY., ZerjalT., BaoW., ZhuS., LimS., ShuQ., XuJ., DuR., FuS., LiP.2005. Recent spread of a Y-chromosomal lineage in Northern China and Mongolia. Am. J. Hum.Genetics., 77:1112–1116.
57.
XueY., ZhangX., HuangN., DalyA., GillsonC.J., MacArthurD.G., YngvadottirB., NicaA.C., WoodwarkC., ChenY.et al.2009. Population differentiation as an indicator of recent positive selection in humans: an empirical evaluation. Genetics., 183:1065–1077.
58.
YangZ., Dos ReisM.2010. Statistical properties of the branch-site test of positive selection. Mol. Biol. Evolution[Epub ahead of print].
59.
YiX., LiangY., Huerta-SanchezE., JinX., CuoZ.X.P., PoolJ.E., XuX., JiangH., VinckenboschN., KorneliussenT.S.et al.2010. Sequencing of 50 human exomes reveals adaptation to high altitude. Science., 329:75–78.
60.
ZerjalT.2003. The genetic legacy of the Mongols. Am. J. Hum. Genetics., 72:717–721.
61.
ZhangC.2006. A whole genome long-range haplotype (WGLRH) test for detecting imprints of positive selection in human populations. Bioinformatics., 22:2122–2128.
