Haplotype trees and modern human origins

Yearbook of Physical Anthropology

Volumn 48, Issue , 2005, Pages 33-59

  Templeton, Alan R ^a  

^a WASHINGTON UNIVERSITY   (United States)

Author keywords

Coalescence; Coevolution; Gene flow; Natural selection; Replacement

Indexed keywords

EID: 32044444659     PISSN: 0096848X     EISSN: None     Source Type: Journal    
DOI: 10.1002/ajpa.20351     Document Type: Review

References (131)

1. Adams AM, Hudson RR. 2004. Maximum-likelihood estimation of demographic parameters using the frequency spectrum of unlinked single-nucleotide polymorphisms. Genetics 168: 1699-1712.
2. Aguirre E, Carbonell E. 2001. Early human expansions into Eurasia: the Atapuerca evidence. Quatern Int 75:11-18.
3. Akey JM, Eberle MA, Rieder MJ, Carlson CS, Shriver MD, Nickerson DA, Kruglyak L. 2004. Population history and natural selection shape patterns of genetic variation in 132 genes. Plos Biol 2:1591-1599.
4. Antón SC, Leonard WR, Robertson ML. 2002. An ecomorphological model of the initial hominid dispersal from Africa. J Hum Evol 43:773-785.
5. Asfaw B, Beyne Y, Suwa G, Walter RC, White TD, WoldeGabriel G, Yemane T. 1992. The earliest Acheulean from Konso-Gardula. Nature 360:732-735.
6. Ashford RW. 2000. Parasites as indicators of human biology and evolution. J Med Microbiol 49:771-772.
7. Avise JC. 2000. Phylogeography. Cambridge, MA: Harvard University Press.
8. Bacon AL, Dunlop MG, Farrington SM. 2001. Hypermutability at a poly(A/T) tract in the human germline. Nucleic Acids Res 29:4405-4413.
9. Bamshad MJ, Wooding SP. 2003. Signatures of natural selection in the human genome. Nat Rev Genet 4:99-111.
10. Bar-Yosef O, Belfer-Cohen A. 2001. From Africa to Eurasia-early dispersals. Quatern Int 75:19-28.
11. Brown P, Sutikna T, Morwood MJ, Soejono RP, Jatmiko, Wayhu Saptomo E, Awe Due R. 2004. A new small-bodied hominin from the late Pleistocene of Flores, Indonesia. Nature 431:1055-1061.
12. Buzin CH, Feng JN, Yan J, Scaringe W, Liu Q, den Dunnen J, Mendell JR, Sommer SS. 2005. Mutation rates in the dystrophin gene: a hotspot of mutation at a CpG dinucleotide. Hum Mutat 25:177-188.
13. Caldararo N, Gabow S. 2000. Mitochondrial DNA analysis and the place of Neandertals in Homo. Ancient Biomol 3:135-158.
14. Cann RL, Stoneking M, Wilson AC. 1987. Mitochondrial DNA and human evolution. Nature 325:31-36.
15. Caramelli D, Lalueza-Fox C, Vernesi C, Lari M, Casoli A, Mallegni F, Chiarelli B, Dupanloup I, Bertranpetit J, Barbujani G, Bertorelle G. 2003. Evidence for a genetic discontinuity between Neandertals and 24,000-year-old anatomically modern Europeans. Proc Natl Acad Sci USA 100:6593-6597.
16. Castelloe J, Templeton AR. 1994. Root probabilities for intraspecific gene trees under neutral coalescent theory. Mol Phylogenet Evol 3:102-113.
17. Clark AG, Glanowski S, Nielsen R, Thomas PD, Kejariwal A, Todd MA, Tanenbaum DM, Civello D, Lu F, Murphy B, Ferriera S, Wang G, Zheng XG, White TJ, Sninsky JJ, Adams MD, Cargill M. 2003. Inferring nonneutral evolution from human-chimp-mouse orthologous gene trios. Science 302:1960-1963.
18. Crandall KA. 1994. Intraspecific cladogram estimation: accuracy at higher levels of divergence. Syst Biol 43:222-235.
19. Crandall KA, Templeton AR. 1993. Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. Genetics 134:959-969.
20. Crandall KA, Templeton AR. 1999. Statistical approaches to detecting recombination. In: Crandall KA, editor. The evolution of HIV. Baltimore: Johns Hopkins University Press. p 153-176.
21. Crawford DC, Bhangale T, Li N, Hellenthal G, Rieder MJ, Nickerson DA, Stephens M. 2004. Evidence for substantial fine-scale variation in recombination rates across the human genome. Nat Genet 36:700-706.
22. Crow JF, Kimura M. 1970. An introduction to population genetic theory. New York: Harpr & Row.
23. Curnoe D, Thorne A. 2003. Number of ancestral human species: a molecular perspective. Homo J Comp Hum Biol 53:201-224.
24. Currat M, Excoffier L. 2004. Modern humans did not admix with Neanderthals during their range expansion into Europe. Plos Biol 2:421.
25. Donnelly P, Tavare S. 1995. Coalescents and genealogical structure under neutrality. Annu Rev Genet 29:401-421.
26. Eller E. 2002. Population extinction and recolonization in human demographic history. Math Biosci 177:1-10.
27. Eller E, Hawks J, Relethford JH. 2004. Local extinction and recolonization, species effective population size, and modern human origins. Hum Biol 76:689-709.
28. Elson JL, Turnbull DM, Howell N. 2004. Comparative genomics and the evolution of human mitochondrial DNA: assessing the effects of selection. Am J Hum Genet 74:229-238.
29. Eswaran V, Harpending H, Rogers AR. 2005. Genomics refutes an exclusively African origin of humans. J Hum Evol 49:1-18.
30. Ewens WJ. 1990. Population genetics theory-the past and the future. In: Lessard S, editor. Mathematical and statistical developments of evolutionary theory. Dordrecht: Kluwer Academic Publishers. p 177-227.
31. Felsenstein J. 2004. Inferring phylogenies. Sunderland, MA: Sinauer Associates, Inc.
32. Forde SE, Thompson JN, Bohannan BJM. 2004. Adaptation varies through space and time in a coevolving host-parasitoid interaction. Nature 431:841-844.
33. Fryxell KJ, Moon W-J. 2005. CpG mutation rates in the human genome are highly dependent on local GC content. Mol Biol Evol 22:650-658.
34. Garrigan D, Mobasher Z, Severson T, Wilder JA, Hammer MF. 2005. Evidence for archaic Asian ancestry on the human X chromosome. Mol Biol Evol 22:189-192.
35. Glenn DR, Brooks DR. 1986. Parasitological evidence pertaining to the phylogeny of the hominid parasites. Biol J Linn Soc 27:331-354.
36. Gutierrez G, Sanchez D, Marin A. 2002. A reanalysis of the ancient mitochondrial DNA sequences recovered from Neandertal bones. Mol Biol Evol 19:1359-1366.
37. Hansen AJ, Willerslev E, Wiuf C, Mourier T, Arctander P. 2001. Statistical evidence for miscoding lesions in ancient DNA templates. Mol Biol Evol 18:262-265.
38. Harpending H, Rogers A. 2000. Genetic perspectives on human origins and differentiation. Annu Rev Genom Hum Genet 1:361-73.
39. Hawks J, Hunley K, Lee S, Wolpoff M. 2000. Population bottlenecks and Pleistocene human evolution. Mol Biol Evol 17:2-22.
40. Hein J, Schierup MH, Wiuf C. 2005. Gene genealogies, variation and evolution: a primer in coalescent theory. Oxford: Oxford University Press.
41. Hoberg EP, Alkire NL, Queiroz Ad, Jones A. 2001. Out of Africa: origins of the Taenia tapeworms in humans. Proc R Soc Lond [Biol] 268:781-787.
42. Hou YM, Potts R, Yuan BY, Guo ZT, Deino A, Wang W, Clark J, Xie GM, Huang WW. 2000. Mid-Pleistocene Acheulean-like stone technology of the Bose Basin, South China. Science 287:1622-1626.
43. Hudson RR. 1990. Gene genealogies and the coalescent process. Oxf Surv Evol Biol 7:1-44.
44. Hutchison DW, Templeton AR. 1999. Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53:1898-1914.
45. Innan H, Zhang K, Marjoram P, Tavare S, Rosenberg NA. 2005. Statistical tests of the coalescent model based on the haplotype frequency distribution and the number of segregating sites. Genetics 169:1763-1777.
46. Joy DA, Feng XR, Mu JB, Furuya T, Chotivanich K, Krettli AU, Ho M, Wang A, White NJ, Suh E, Beerli P, Su XZ. 2003. Early origin and recent expansion of Plasmodium falciparum. Science 300:318-321.
47. Kimura M. 1970. The length of time required for a selectively neutral mutant to reach fixation through random frequency drift in a finite population. Genet Res 15:131-133.
48. Knight A. 2003. The phylogenetic relationship of Neandertal and modern human mitochondrial DNAs based on informative nucleotide sites. J Hum Evol 44:627-632.
49. Knowles LL, Maddison WP. 2002. Statistical phylogeography. Mol Ecol 11:2623-2635.
50. Krings M, Capelli C, Tschentscher F, Geisert H, Meyer S, Haesler Av, GrossSchmitz K, Possnert G, Paunovic M, Pääbo S. 2000. A view of Neandertal genetic diveresity. Nat Genet 26:144-146.
51. Lalueza-Fox C, Sampietro ML, Caramelli D, Puder Y, Lari M, Calafell F, Martinez-Maza C, Bastir M, Fortea J, Rasilla Mdl, Bertranpetit J, Rosas A. 2005. Neandertal evolutionary genetics: mitochondrial DNA data from the Iberian Peninsula. Mol Biol Evol 22:1077-1081.
52. Lercher MJ, Hurst LD. 2002. Human SNP variability and mutation rate are higher in regions of high recombination. TIG 18:337-340.
53. Lordkipanidze D, Vekua A, Ferring R, Rightmire GP, Agusti J, Kiladze G, Mouskhelishvili A, Nioradze M, de Leon MSP, Tappen M, Zollikofer CPE. 2005. Anthropology: the earliest toothless hominin skull. Nature 434:717.
54. Marth G, Schuler G, Yeh R, Davenport R, Agarwala R, Church D, Wheelan S, Baker J, Ward M, Kholodov M, Phan L, Czabarka E, Murvai J, Cutler D, Wooding S, Rogers A, Chakravarti A, Harpending HC, Kwok P-Y, Sherry ST. 2003. Sequence variations in the public human genome data reflect a bottlenecked population history. Proc Natl Acad Sci USA 100:376-381.
55. Marth GT, Czabarka E, Murvai J, Sherry ST. 2004. The allele frequency spectrum in genome-wide human variation data reveals signals of differential demographic history in three large world populations. Genetics 166:351-372.
56. McVean GAT, Myers SR, Hunt S, Deloukas P, Bentley DR, Donnelly P. 2004. The fine-scale structure of recombination rate variation in the human genome. Science 304:581-584.
57. Nordborg M. 1998. On the probability of Neanderthal ancestry. Am J Hum Genet 63:1237-1240.
58. Palsboll PJ, Berube M, Aguilar A, Notarbartolo-Di-Sciara G, Nielsen R. 2004. Discerning between recurrent gene flow and recent divergence under a finite-site mutation model applied to North Atlantic and Mediterranean Sea fin whale (Balaenoptera physalus) populations. Evolution 58:670-675.
59. Pavesi A. 2004. Detecting traces of prehistoric human migrations by geographic synthetic maps of polyomavirus JC. J Mol Evol 58:304-313.
60. Pearson OM. 2004. Has the combination of genetic and fossil evidence solved the riddle of modern human origins? Evol Anthropol 13:145-159.
61. Pellmyr O. 2003. Yuccas, yucca moths, and coevolution: a review. Ann Mo Bot Gard 90:35-55.
62. Perlman SJ, Jaenike J. 2003. Infection success in novel hosts: an experimental and phylogenetic study of Drosophila-parasitic nematodes. Evolution 57:544-557.
63. Pluzhnikov A, Di Rienzo A, Hudson RR. 2002. Inferences about human demography based on multilocus analyses of noncoding sequences. Genetics 161:1209-1218.
64. Posada D. 2002. Evaluation of methods for detecting recombination from DNA sequences: empirical data. Mol Biol Evol 19:708-717.
65. Posada D, Buckley TR. 2004. Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793-808.
66. Posada D, Crandall KA. 1998. ModelTest: testing the model of DNA substitution. Bioinformatics 14:817-818.
67. Posada D, Crandall KA. 2001. Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci USA 98:13757-13762.
68. Posada D, Crandall KA. 2002. The effect of recombination on the accuracy of phylogeny estimation. J Mol Evol 54:396-402.
69. Posada D, Crandall KA, Holmes EC. 2002. Recombination in evolutionary genomics. Annu Rev Genet 36:75-97.
70. Pusch CM, Bachmann L. 2004. Spiking of contemporary human template DNA with ancient DNA extracts induces mutations under PCR and generates nonauthentic mitochondrial sequences. Mol Biol Evol 21:957-964.
71. Rannala B, Bertorelle G. 2001. Using linked markers to infer the age of a mutation. Hum Mutat 18:87-100.
72. Ray N, Currat M, Berthier P, Excoffier L. 2005. Recovering the geographic origin of early modern humans by realistic and spatially explicit simulations. Genome Res 15:1161-1167.
73. Reed DL, Smith VS, Hammond SL, Rogers AR, Clayton DH. 2004. Genetic analysis of lice supports direct contact between modern and archaic humans. Plos Biol 2:340.
74. Relethford JH. 2001a. Absence of regional affinities of Neandertal DNA with living humans does not reject multiregional evolution. Am J Phys Anthropol 115:95-98.
75. Relethford JH. 2001b. Genetics and the search for modern human origins. New York: John Wiley & Sons.
76. Ricaut FX, Fedoseeva A, Keyser-Tracqui C, Crubezy E, Ludes B. 2005. Ancient DNA analysis of human Neolithic remains found in northeastern Siberia. Am J Phys Anthropol 126:458-462.
77. Richards M. 2003. The Neolithic invasion of Europe. Annu Rev Anthropol 32:135-162.
78. Richards M, Macaulay V, Hickey E, Vega E, Sykes B, Guida V, Rengo C, Sellitto D, Cruciani F, Kivisild T, Villems R, Thomas M, Rychkov S, Rychkov O, Rychkov Y, Gölge M, Dimitrov D, Hill E, Bradley D, Romano V, Calì F, Vona G, Demaine A, Papiha S, Triantaphyllidis C, Stefanescu G, Hatina J, Belledi M, Rienzo AD, Novelletto A, Oppenheim A, Nørby S, Al-Zaheri N, Santachiara-Benerecetti S, Scozzari R, Torroni A, Bandelt H-J. 2000. Tracing European founder lineages in the Near Eastern mtDNA pool. Am J Hum Genet 67:1251-1276.
79. Rightmire GP. 2004. Brain size and encephalization in early to mid-Pleistocene Homo. Am J Phys Anthropol 124:109-123.
80. Rogers AR, Praley AE, Bamshad MJ, Watkins WS, Jorde LB. 1996. Mitochondrial mismatch analysis is insensitive to the mutational process. Mol Biol Evol 13:895-902.
81. Ruff CB, Trinkaus E, Holliday TW. 1997. Body mass and encephalization in Pleistocene Homo. Nat 387:173-176.
82. Schneider S, Excoffier L. 1999. Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates very among sites: application to human mitochondrial DNA. Genetics 152:1079-1089.
83. Segraves KA, Pellmyr O. 2004. Testing the out-of-Florida hypothesis on the origin of cheating in the yucca-yucca moth mutualism. Evolution 58:2266-2279.
84. Serre D, Langaney A, Chech M, Teschler-Nicola M, Paunovic M, Mennecier P, Hofreiter M, Possnert G, Pääbo S. 2004. No evidence of Neandertal mtDNA contribution to early modern humans. Plos Biol 2:313-317.
85. Sharp PM, Bailes E, Chaudhuri RR, Rodenburg CM, Santiago MO, Hahn BH. 2001. The origins of acquired immune deficiency syndrome viruses: where and when? Philos Trans R Soc Lond [Biol] 356.
86. Shingleton AW, Stern DL. 2003. Molecular phylogenetic evidence for multiple gains or losses of ant mutualism within the aphid genus Chaitophorus. Mol Phylogenet Evol 26:26-35.
87. Soodyall H. 1993. Mitochondrial DNA polymorphisms in southern African populations. Ph.D. thesis, University of the Witwatersrand, Johannesburg.
88. Stephens M, Smith NJ, Donnelly P. 2001. A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978-989.
89. Stoneking M, Jorde LB, Bhatia K, Wilson AC. 1990. Geographic variation in human mitochondrial DNA from Papua New Guinea. Genetics 124:717-733.
90. Storz JF, Payseur BA, Nachman MW. 2004. Genome scans of DNA variability in humans reveal evidence for selective sweeps outside of Africa. Mol Biol Evol 21:1800-1811.
91. Stringer C. 2002. Modern human origins: progress and prospects. Philos Trans R Soc Lond [Biol] 357:563-579.
92. Stringer CB, Andrews P. 1988. The origin of modern humans. Science 239:1263-1268.
93. Sykes B, Leiboff A, Low-Beer J, Tetzner S, Richards M. 1995. The origins of the Polynesians: an interpretation from mitochondrial lineage analysis. Am J Hum Genet 57:1463-1475.
94. Tajima F. 1983. Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437-460.
95. Tajima F. 1989a. The effect of change in population size on DNA polymorphism. Genetics 123:597-601.
96. Tajima F. 1989b. Statistical-method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585.
97. Templeton AR. 1993. The "Eve" hypothesis: a genetic critique and reanalysis. Am Anthropol 95:51-72.
98. Templeton AR. 1994. "Eve:" hypothesis compatibility versus hypothesis testing. Am Anthropol 96:141-147.
99. Templeton AR. 1996. Contingency tests of neutrality using intra/interspecific gene trees: the rejection of neutrality for the evolution of the mitochondrial cytochrome oxidase II gene in the hominoid primates. Genetics 144:1263-1270.
100. Templeton AR. 1998. Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history. Mol Ecol 7:381-397.
101. Templeton AR. 2002. Out of Africa again and again. Nature 416:45-51.
102. Templeton AR. 2004a. A maximum likelihood framework for cross validation of phylogeographic hypotheses. In: Wasser SP, editor. Evolutionary theory and processes: modern horizons. Dordrecht: Kluwer Academic Publishers. p 209-230.
103. Templeton AR. 2004b. Statistical phylogeography: methods of evaluating and minimizing inference errors. Mol Ecol 13:789-809.
104. Templeton AR. 2005. Population biology and population genetics of Pleistocene hominins. In: Henke W, Rothe H, Tattersall I, editors. Handbook of palaeoanthropology. Berlin: Springer-Verlag. In press.
105. Templeton AR, Sing CF. 1993. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. IV. Nested analyses with cladogram uncertainty and recombination. Genetics 134:659-669.
106. Templeton AR, Boerwinkle E, Sing CF. 1987. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. I. Basic theory and an analysis of alcohol dehydrogenase activity in Drosophila. Genetics 117:343-351.
107. Templeton AR, Sing CF, Kessling A, Humphries S. 1988. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. II. The analysis of natural populations. Genetics 120:1145-1154.
108. Templeton AR, Crandall KA, Sing CF. 1992. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619-633.
109. Templeton AR, Routman E, Phillips C. 1995. Separating population structure from population history: a cladistic analysis of the geographical distribution of mitochondrial DNA haplotypes in the tiger salamander, Ambystoma tigrinum. Genetics 140:767-782.
110. Templeton AR, Clark AG, Weiss KM, Nickerson DA, Boerwinkle E, Sing CF. 2000a. Recombinational and mutational hotspots within the human Lipoprotein Lipase gene. Am J Hum Genet 66:69-83.
111. Templeton AR, Weiss KM, Nickerson DA, Boerwinkle E, Sing CF. 2000b. Cladistic structure within the human Lipoprotein Lipase gene and its implications for phenotypic association studies. Genetics 156:1259-1275.
112. Thomas MG, Parfitt T, Weiss DA, Skorecki K, Wilson JF, Roux ML, Bradman N, Goldstein DB. 2000. Y chromosomes traveling south: the Cohen modal haplotype and the origins of the Lemba-the "Black Jews of Southern Africa." Am J Hum Genet 66:674-686.
113. Tishkoff SA, Verrelli BC. 2003. Patterns of human genetic diversity: implications for human evolutionary history and disease. Annu Rev Genom Hum Genet 4:293-340.
114. Tomatsu S, Orii KO, Bi Y, Gutierrez MA, Nishioka T, Yamaguchi S, Kondo N, Orii T, Noguchi A, Sly WS. 2004. General implications for CpG hot spot mutations: methylation patterns of the human iduronate-2-sulfatase gene locus. Hum Mutat 23:590-598.
115. Tomso DJ, Bell DA. 2003. Sequence context at human single nucleotide polymorphisms: overrepresentation of CpG dinucleotide at polymorphic sites and suppression of variation in CpG islands. J Mol Biol 327:303-308.
116. Torroni A, Schurr TG, Cabell MF, Brown MD, Neel JV, Larsen M, Smith DG, Vullo CM, Wallace DC. 1993a. Asian affinities and continental radiation of the four founding Native American mtDNAs. Am J Hum Genet 53:563-590.
117. Torroni A, Sukernik RI, Schurr TG, Starikovskaya YB, Cabell MF, Crawford MH, Comuzzie AG, Wallace DC. 1993b. mtDNA variation of aboriginal Siberians reveals distinct genetic affinities with Native Americans. Am J Hum Genet 53:591-608.
118. Tsaousis AD, Martin DP, Ladoukakis ED, Posada D, Zouros E. 2005. Widespread recombination in published animal mtDNA sequences. Mol Biol Evol 22:925-933.
119. Vallender EJ, Lahn BT. 2004. Positive selection on the human genome. Hum Mol Genet 13:245-R254.
120. Vekua A, Lordkipanidze D, Rightmire GP, Agusti J, Ferring R, Maisuradze G, Mouskhelishvili A, Nioradze M, de Leon MP, Tappen M, Tvalchrelidze M, Zollikofer C. 2002. A new skull of early Homo from Dmanisi, Georgia. Science 297:85-89.
121. Vigilant L, Stoneking M, Harpending H, Hawkes K, Wilson AC. 1991. African populations and the evolution of human mitochondrial DNA. Science 253:1503-1507.
122. Volkman SK, Barry AE, Lyons EJ, Nielsen KM, Thomas SM, Choi M, Thakore SS, Day KP, Wirth DF, Hartl DL. 2001. Recent origin of Plasmodium falciparum from a single progenitor. Science 293:482-484.
123. Wall JD. 2000. Detecting ancient admixture in humans using sequence polymorphism data. Genetics 154:1271-1279.
124. Weiss KM. 1984. On the numbers of members of the genus Homo who have ever lived, and some evolutionary implications. Hum Biol 56:637-649.
125. White TD, Asfaw B, DeGusta D, Gilbert H, Richards GD, Suwa G, Howell FC. 2003. Pleistocene Homo sapiens from Middle Awash, Ethiopia. Nature 423:742-747.
126. Willerslev E, Cooper A. 2005. Ancient DNA. Proc R Soc Lond [Biol] 272:3-16.
127. Wilson JF, Goldstein DB. 2000. Consistent long-range linkage disequilibrium generated by admixture in a Bantu-Semitic hybrid population. Am J Hum Genet 67:926-935.
128. Wooding S, Rogers A. 2002. The matrix coalescent and an application to human single-nucleotide polymorphisms. Genetics 161:1641-1650.
129. Yang Z. 1997. On the estimation of ancestral population sizes of modern humans. Genet Res 69:111-116.
130. Zangerl AR, Berenbaum MR. 2003. Phenotype matching in wild parsnip and parsnip webworms: causes and consequences. Evolution 57:806-815.
131. Zhao Z, Boerwinkle E. 2002. Neighboring-nucleotide effects on single nucleotide polymorphisms: a study of 2.6 million polymorphisms across the human genome. Genome Res 12:1679-1686.