, Volume 135, Issue 3, pp 439–455 | Cite as

Multilocus phylogeography and phylogenetics using sequence-based markers

  • Patrícia H. Brito
  • Scott V. Edwards


We review recent trends in phylogeography and phylogenetics and argue that these two fields stand to be reunited by the common yardstick provided by sequence and SNP data and by new multilocus methods for phylogenetic analysis. Whereas the modern incarnation of both fields was spawned by PCR approaches applied to mitochondrial DNA in the late 1980s, the two fields diverged during the 1990s largely due to the adoption by phylogeographers of microsatellites, in contrast to the adoption of nuclear sequence data by phylogeneticists. Sequence-based markers possess a number of advantages over microsatellites, even on the recent time scales that are the purview of phylogeography. Using examples primarily from vertebrates, we trace the maturation of nuclear gene phylogeography and phylogenetics and suggest that the abundant instances of gene tree heterogeneity beckon a new generation of phylogenetic methods that focus on estimating species trees as distinct from gene trees. Whole genomes provide a powerful common yardstick on which both phylogeography and phylogenetics can assume their proper place as ends of a continuum.


Multilocus analysis Indel Intron Genomic phylogeography SNP Species tree 



PHB was supported by a postdoctoral fellowship awarded by the Fundação para a Ciência e Tecnologia, Portugal. We thank our lab colleagues and Carlos Bustamante for helpful discussion. We are grateful for the criticisms of two anonymous reviewers and to Craig Moritz and Rauri Bowie for their perspective and for providing detailed comments on the manuscript.


  1. Avise JC (2000) Phylogeography. The history and formation of species. Harvard University Press, Cambridge, MassachusettsGoogle Scholar
  2. Avise JC, Ball RM Jr (1990) Principles of genealogical concordance in species concepts and biological taxonomy. Oxf Surv Evol Biol 7:45–67Google Scholar
  3. Avise JC, Arnold J, Ball RM et al (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst 18:489–522Google Scholar
  4. Backström N, Fagerberg S, Ellegren H (2008) Genomics of natural bird populations: a gene-based set of reference markers evenly spread across the avian genome. Mol Ecol 17:964–980. doi: 10.1111/j.1365-294X.2007.03551.x PubMedGoogle Scholar
  5. Bazin E, Glémin S, Galtier N (2006) Population size does not influence mitochondrial genetic diversity in animals. Science 312:570–572. doi: 10.1126/science.1122033 PubMedGoogle Scholar
  6. Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc R Soc Lond B Biol Sci 263:1619–1626. doi: 10.1098/rspb.1996.0237 Google Scholar
  7. Beaumont MA, Rannala B (2004) The Bayesian revolution in genetics. Nat Rev Genet 5:251–261. doi: 10.1038/nrg1318 PubMedGoogle Scholar
  8. Beaumont MA, Zhang W, Balding DJ (2002) Approximate bayesian computation in population genetics. Genetics 162:2025–2035PubMedGoogle Scholar
  9. Becquet C, Przeworski M (2007) A new approach to estimate parameters of speciation models with application to apes. Genome Res 17:1505–1519. doi: 10.1101/gr.6409707 PubMedGoogle Scholar
  10. Beerli P, Felsenstein J (1999) Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics 152:763–773PubMedGoogle Scholar
  11. Belfiore NM, Liu L, Moritz C (2008) Multilocus phylogenetics of a rapid radiation in the genus thomomys (Rodentia: Geomyidae). Syst Biol 57:294–310. doi: 10.1080/10635150802044011 PubMedGoogle Scholar
  12. Benavides E, Baum R, McClellan D, Sites JW Jr (2007) Molecular phylogenetics of the lizard genus Microlophus (Squamata: Tropiduridae): aligning and retrieving indel signal from nuclear introns. Syst Biol 56:776–797. doi: 10.1080/10635150701618527 PubMedGoogle Scholar
  13. Bensch S, Irwin DE, Irwin JH, Kvist L, Åkesson S (2006) Conflicting patterns of mitochondrial and nuclear DNA diversity in Phylloscopus warblers. Mol Ecol 15:161–171. doi: 10.1111/j.1365-294X.2005.02766.x PubMedGoogle Scholar
  14. Berlin S, Tomaras D, Charlesworth B (2007) Low mitochondrial variability in birds may indicate Hill-Robertson effects on the W chromosome. Heredity 99:389–396. doi: 10.1038/sj.hdy.6801014 PubMedGoogle Scholar
  15. Binladen J, Thomas M, Gilbert P et al (2007) The use of coded PCR primers enables high-throughput sequencing of multiple homolog amplification products by 454 parallel sequencing. PLoS One 2:e197. doi: 10.1371/journal.pone.0000197
  16. Black WC, Baer CF, Antolin MF, DuTeau NM (2001) Population genomics: genome-wide sampling of insect populations. Annu Rev Entomol 46:441–469. doi: 10.1146/annurev.ento.46.1.441 PubMedGoogle Scholar
  17. Boissinot S, Chevret P, Furano AV (2000) L1 (LINE–1) retrotransposon evolution and amplification in recent human history. Mol Biol Evol 17:915–928PubMedGoogle Scholar
  18. Bourque G, Pevzner PA (2002) Genome-scale evolution: reconstructing gene orders in the ancestral species. Genome Res 12:26–36PubMedGoogle Scholar
  19. Bowers JE, Chapman BA, Rong J, Paterson AH (2003) Unraveling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422:433–438. doi: 10.1038/nature01521 PubMedGoogle Scholar
  20. Brandström M, Ellegren H (2007) The genomic landscape of short insertion and deletion polymorphisms in the chicken (Gallus gallus) genome: a high frequency of deletions in tandem duplicates. Genetics 176:1691–1701. doi: 10.1534/genetics.107.070805 PubMedGoogle Scholar
  21. Brown MW, George M Jr, Wilson AC (1979) Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci USA 76:1967–1971. doi: 10.1073/pnas.76.4.1967 PubMedGoogle Scholar
  22. Brumfield RT, Beerli P, Nickerson DA, Edwards SV (2003) The utility of single nucleotide polymorphisms in inferences of population history. Trends Ecol Evol 18:249–256. doi: 10.1016/S0169-5347(03)00018-1 Google Scholar
  23. Bull JJ, Huelsenbeck JP, Cunningham CW, Swofford DL, Waddell PJ (1993) Partitioning and combining data in phylogenetic analysis. Syst Biol 42:384–397. doi: 10.2307/2992473 Google Scholar
  24. Caccone A, Amato GD, Powell JR (1988) Rates and patterns of scnDNA and mtDNA divergence within the Drosophila melanogaster subgroup. Genetics 118:671–683Google Scholar
  25. Carling MD, Brumfield RT (2007) Gene sampling strategies for multi-locus population estimates of genetic diversity (θ). PLoS One 2:e160. doi: 10.1371/journal.pone.0000160
  26. Carling MD, Brumfield RT (2008) Integrating phylogenetic and population genetic analyses of multiple loci to test species divergence hypotheses in Passerina buntings. Genetics 178:363–377. doi: 10.1534/genetics.107.076422 PubMedGoogle Scholar
  27. Carstens BC, Knowles LL (2007a) Estimating species phylogeny from gene-tree probabilities despite incomplete lineage sorting: an example from Melanoplus grasshoppers. Syst Biol 56:400–411. doi: 10.1080/10635150701405560 PubMedGoogle Scholar
  28. Carstens BC, Knowles LL (2007b) Shifting distributions and speciation: species divergence during rapid climate change. Mol Ecol 16:619–627. doi: 10.1111/j.1365-294X.2006.03167.x PubMedGoogle Scholar
  29. Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Evol Int J Org Evol 32:550–570. doi: 10.2307/2406616 Google Scholar
  30. Chen FC, Li WH (2001) Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees. Am J Hum Genet 68:444–456. doi: 10.1086/318206 PubMedGoogle Scholar
  31. Cummings MP, Otto SP, Wakeley J (1995) Sampling properties of DNA sequence data in phylogenetic analysis. Mol Biol Evol 12:814–822PubMedGoogle Scholar
  32. Delsuc F, Brinkmann H, Philippe H (2005) Phylogenomics and the reconstruction of the tree of life. Nat Rev Genet 6:361–375. doi: 10.1038/nrg1603 PubMedGoogle Scholar
  33. Dettman JR, Jacobson DJ, Taylor JW (2003) A multilocus genealogical approach to phylogenetic species recognition in the model eukaryote Neurospora. Evol Int J Org Evol 57:2703–2720Google Scholar
  34. Dolman G, Moritz C (2006) A multilocus perspective on refugial isolation and divergence in rainforest skinks (Carlia). Evol Int J Org Evol 60:573–582Google Scholar
  35. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214. doi: 10.1186/1471–2148-7-214 PubMedGoogle Scholar
  36. Edwards SV (1993) Long-distance gene flow in a cooperative breeder detected in genealogies of mitochondrial DNA sequences. Proc R Soc Lond B Biol Sci 252:177–185. doi: 10.1098/rspb.1993.0063 Google Scholar
  37. Edwards SV, Beerli P (2000) Perspective: gene divergence, population divergence, and the variance in coalescence time in phylogeographic studies. Evol Int J Org Evol 54:1839–1854Google Scholar
  38. Edwards SV, Jennings WB, Shedlock AM (2005) Phylogenetics of modern birds in the era of genomics. Proc R Soc Lond B Biol Sci 272:979–992. doi: 10.1098/rspb.2004.3035 Google Scholar
  39. Edwards SV, Liu L, Pearl DK (2007) High-resolution species trees without concatenation. Proc Natl Acad Sci USA 104:5936–5941. doi: 10.1073/pnas.0607004104 PubMedGoogle Scholar
  40. Ellegren H (2004) Microsatellites: simple sequences with complex evolution. Nat Rev Genet 5:435–445. doi: 10.1038/nrg1348 PubMedGoogle Scholar
  41. Ewens WJ (1972) The sampling theory of selectively neutral alleles. Theor Popul Gen 3:87–112. doi: 10.1016/0040-5809(72)90035-4 Google Scholar
  42. Ewing GB, Ebersberger I, Schmidt HA, von Haeseler A (2008) Rooted triple consensus and anomalous gene trees. BMC Evol Biol 8:118PubMedGoogle Scholar
  43. Fan JB, Oliphant A, Shen R et al (2003) Highly parallel SNP genotyping. Cold Spring Harb Symp Quant Biol 68:69–78. doi: 10.1101/sqb.2003.68.69
  44. Felsenstein J (1981) Evolutionary trees from gene frequencies and quantitative characters: finding maximum likelihood estimates. Evol Int J Org Evol 35:1229–1242. doi: 10.2307/2408134 Google Scholar
  45. Felsenstein J (2006) Accuracy of coalescent likelihood estimates: do we need more sites, more sequences, or more loci? Mol Biol Evol 23:691–700. doi: 10.1093/molbev/msj079 PubMedGoogle Scholar
  46. Friesen V, Congdon B, Walsh H, Birt T (1997) Intron variation in marbled murrelets detected using analyses of single-stranded conformational polymorphisms. Mol Ecol 6:1047–1058. doi: 10.1046/j.1365-294X.1997.00277.x PubMedGoogle Scholar
  47. Funk DJ, Omland KE (2003) Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annu Rev Ecol Evol Syst 34:397–423. doi: 10.1146/annurev.ecolsys.34.011802.132421 Google Scholar
  48. Hare MP (2001) Prospects for nuclear gene phylogeography. Trends Ecol Evol 16:700–706. doi: 10.1016/S0169-5347(01)02326-6 Google Scholar
  49. Hare M, Avise J (1998) Population structure in the American oyster as inferred by nuclear gene genealogies. Mol Biol Evol 15:119–128Google Scholar
  50. Harpending HC, Batzer MA, Gurven M et al (1998) Genetic traces of ancient demography. Proc Natl Acad Sci USA 95:1961–1967. doi: 10.1073/pnas.95.4.1961 PubMedGoogle Scholar
  51. Harr B, Kauer M, Schlötterer C (2002) Hitchhiking mapping—a population-based fine mapping strategy for adaptive mutations in Drosophila melanogaster. Proc Natl Acad Sci USA 99:12949–12954. doi: 10.1073/pnas.202336899 PubMedGoogle Scholar
  52. Hedrick PW (1999) Perspective: highly variable loci and their interpretation in evolution and conservation. Evol Int J Org Evol 53:313–318. doi: 10.2307/2640768 Google Scholar
  53. Hedrick PW (2005) A standardized genetic differentiation measure. Evol Int J Org Evol 59:1633–1638Google Scholar
  54. Hernandez RD, Hubisz MJ, Wheeler DA et al (2007) Demographic histories and patterns of linkage disequilibrium in Chinese and Indian rhesus macaques. Science 316:240–243. doi: 10.1126/science.1140462 PubMedGoogle Scholar
  55. Hey J, Machado CA (2003) The study of structured populations—new hope for a difficult and divided science. Nat Rev Genet 4:535–543. doi: 10.1038/nrg1112 PubMedGoogle Scholar
  56. Hey J, Nielsen R (2004) Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167:747–760. doi: 10.1534/genetics.103.024182 PubMedGoogle Scholar
  57. Hey J, Nielsen R (2007) Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proc Natl Acad Sci USA 104:2785–2790. doi: 10.1073/pnas.0611164104 PubMedGoogle Scholar
  58. Hickerson MJ, Stahl E, Takebayashi N (2007) msBayes: pipeline for testing comparative phylogeographic histories using hierarchical approximate Bayesian computation. BMC Bioinformatics 26(8):268Google Scholar
  59. Hudson RR (1992) Gene trees, species trees and the segregation of ancestral alleles. Genetics 131:509–513PubMedGoogle Scholar
  60. Hudson RR, Coyne JA (2002) Mathematical consequences of the genealogical species concept. Evol Int J Org Evol 56:1557–1565Google Scholar
  61. Hudson RR, Kaplan NL (1985) Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111:147–164PubMedGoogle Scholar
  62. Huelsenbeck JP (1996) A likelihood ratio test to detect conflicting phylogenetic signal. Syst Biol 45:92–98. doi: 10.2307/2413514 Google Scholar
  63. Innan H, Stephan W (2000) The coalescent in an exponentially growing metapopulation and its application to Arabidopsis thaliana. Genetics 155:2015–2019PubMedGoogle Scholar
  64. Jennings WB, Edwards SV (2005) Speciational history of Australian grass finches (Poephila) inferred from thirty gene trees. Evol Int J Org Evol 59:2033–2047Google Scholar
  65. Jorde LB, Rogers AR, Watkins WS et al (1997) Microsatellite diversity and the demographic history of modern humans. Proc Natl Acad Sci USA 94:3100–3103. doi: 10.1073/pnas.94.7.3100 PubMedGoogle Scholar
  66. Karl SA, Avise JC (1993) PCR-based assays of mendelian polymorphisms from anonymous single-copy nuclear DNA: techniques and applications for population genetics. Mol Biol Evol 10:342–361PubMedGoogle Scholar
  67. Keightley PD, Johnson T (2004) MCALIGN: stochastic alignment of non-coding DNA sequences based on an evolutionary model of sequence evolution. Genome Res 14:442–450. doi: 10.1101/gr.1571904 PubMedGoogle Scholar
  68. Kingman JFC (1982a) On the genealogy of large populations. J Appl Probab A 19:27–43. doi: 10.2307/3213548 Google Scholar
  69. Kingman JFC (1982b) The coalescent. Stochast Process Appl 13:235–248. doi: 10.1016/0304-4149(82)90011-4 Google Scholar
  70. Kluge AG (1989) A concern for evidence and a phylogenetic hypothesis of relationships among Epicrates (Boidae, Serpentes). Syst Zool 38:7–25. doi: 10.2307/2992432 Google Scholar
  71. Knowles LL, Maddison WP (2002) Statistical phylogeography. Mol Ecol 11:2623–2635. doi: 10.1046/j.1365-294X.2002.01637.x Google Scholar
  72. Knowles LL, Carstens BC (2007a) Delimiting species without monophyletic gene trees. Syst Biol 56:887–895. doi: 10.1080/10635150701701091 PubMedGoogle Scholar
  73. Knowles LL, Carstens BC (2007b) Estimating a geographically explicit model of population divergence. Evol Int J Org Evol 61:477–493. doi: 10.1111/j.1558-5646.2007.00043.x Google Scholar
  74. Kocher TD, Thomas WK, Meyer A et al (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci USA 86:6196–6200. doi: 10.1073/pnas.86.16.6196 PubMedGoogle Scholar
  75. Konkel MK, Wang JX, Liang P, Batzer MA (2007) Identification and characterization of novel polymorphic LINE-1 insertions through comparison of two human genome sequence assemblies. Gene 390:28–38. doi: 10.1016/j.gene.2006.07.040 PubMedGoogle Scholar
  76. Kubatko LS, Degnan JH (2007) Inconsistency of phylogenetic estimates from concatenated data under coalescence. Syst Biol 56:17–24. doi: 10.1080/10635150601146041 PubMedGoogle Scholar
  77. Kuhner MK (2006) LAMARC 2.0: maximum likelihood and Bayesian estimation of population parameters. Bioinformatics 22:768–770. doi: 10.1093/bioinformatics/btk051 PubMedGoogle Scholar
  78. Kuhner MK, Yamato J, Felsenstein J (1998) Maximum likelihood estimation of population growth rates based on the coalescent. Genetics 149:429–434PubMedGoogle Scholar
  79. Ladoukakis ED, Zouros E (2001a) Recombination in animal mitochondrial DNA: evidence from published sequences. Mol Biol Evol 18:2127–2131PubMedGoogle Scholar
  80. Ladoukakis ED, Zouros E (2001b) Direct evidence for homologous recombination in mussel (Mytilus galloprovincialis) mitochondrial DNA. Mol Biol Evol 18:1168–1175PubMedGoogle Scholar
  81. Leigh JW, Susko E, Baumgartner M, Roger AJ (2008) Testing congruence in phylogenomic analysis. Syst Biol 57:104–115. doi: 10.1080/10635150801910436 PubMedGoogle Scholar
  82. Liu L (2006) Reconstructing posterior distributions of a species phylogeny using estimated gene tree distributions, Doctoral dissertation, The Ohio State UniversityGoogle Scholar
  83. Liu L, Pearl DK (2007) Species trees from gene trees: reconstructing Bayesian posterior distributions of a species phylogeny using estimated gene tree distributions. Syst Biol 56:504–514. doi: 10.1080/10635150701429982 PubMedGoogle Scholar
  84. Liu L, Pearl DK, Brumfield RT, Edwards SV (2008) Estimating species trees using multiple-allele DNA sequence data. Evol Int J Org Evol (in press)Google Scholar
  85. Luikart G, England PR, Tallmon D, Jordan S, Taberlet P (2003) The power and promise of population genomics: from genotyping to genome typing. Nat Rev Genet 4:981–994. doi: 10.1038/nrg1226 PubMedGoogle Scholar
  86. Machado CA, Hey J (2003) The causes of phylogenetic conflict in a classic Drosophila species group. Proc R Soc Lond B Biol Sci 270:1193–1202. doi: 10.1098/rspb.2003.2333 Google Scholar
  87. Machado CA, Kliman RM, Markert JA, Hey J (2002) Inferring the history of speciation from multilocus DNA sequence data: the case of Drosophila pseudoobscura and close relatives. Mol Biol Evol 19:472–488PubMedGoogle Scholar
  88. Maddison W (1997) Gene trees in species trees. Syst Biol 46:523–536. doi: 10.2307/2413694 Google Scholar
  89. Maddison W, Knowles LL (2006) Inferring phylogeny despite incomplete lineage sorting. Syst Biol 55:21–30. doi: 10.1080/10635150500354928 PubMedGoogle Scholar
  90. Meyer M, Stenzel U, Myles S, Prüfer K, Hofreiter M (2007) Target high-throughput sequencing of tagged nucleic acid samples. Nucleic Acids Res 35:e97. doi: 10.1093/nar/gkm566
  91. Miklos I, Lunter GA, Holmes I (2004) A “long-indel” model for evolutionary sequence alignment. Mol Biol Evol 21:529–540. doi: 10.1093/molbev/msh043 PubMedGoogle Scholar
  92. Mills RE, Luttig CT, Larkins CE et al (2006) An initial map of insertion and deletion (INDEL) variation in the human genome. Genome Res 16:1182–1190. doi: 10.1101/gr.4565806 PubMedGoogle Scholar
  93. Moore W (1995) Inferring phylogenies from mtDNA variation: mitochondrial-gene trees versus nuclear-gene trees. Evol Int J Org Evol 49:718–726. doi: 10.2307/2410325 Google Scholar
  94. Müller S, Hollatz M, Wienberg J (2003) Chromosomal phylogeny and evolution of gibbons (Hylobatidae). Hum Genet 113:1432–1203. doi: 10.1007/s00439-003-0997-2 Google Scholar
  95. Murphy WJ, Pringle TH, Crider TA, Springer MS, Miller W (2007) Using genomic data to unravel the root of the placental mammal phylogeny. Genome Res 17:413–421. doi: 10.1101/gr.5918807 PubMedGoogle Scholar
  96. Nachman MW (2001) Single nucleotide polymorphisms and recombination rate in humans. Trends Genet 17:481–485. doi: 10.1016/S0168-9525(01)02409-X PubMedGoogle Scholar
  97. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  98. Nielsen R (1998) Maximum likelihood estimation of population divergence times and population phylogenies under the infinite sites model. Theor Popul Biol 53:143–151. doi: 10.1006/tpbi.1997.1348 PubMedGoogle Scholar
  99. Nielsen R, Wakeley J (2001) Distinguishing migration from isolation: a Markov Chain Monte Carlo approach. Genetics 158:885–896PubMedGoogle Scholar
  100. Nielsen R, Mountain JL, Huelsenbeck JP, Slatkin M (1998) Maximum likelihood estimation of population divergence times and population phylogeny in models without mutation. Evol Int J Org Evol 52:669–677. doi: 10.2307/2411262 Google Scholar
  101. Nielsen R, Hubisz MJ, Clark AG (2004) Reconstituting the frequency spectrum of ascertained single-nucleotide polymorphism data. Genetics 168:2373–2382. doi: 10.1534/genetics.104.031039 PubMedGoogle Scholar
  102. Nishihara H, Satta Y, Nikaido M et al (2005) A retroposon analysis of Afrotherian phylogeny. Mol Biol Evol 22:1823–1833. doi: 10.1093/molbev/msi179 PubMedGoogle Scholar
  103. Nylander JAA, Ronquist F, Huelsenbeck JP, Nieves-Aldrey JL (2004) Bayesian phylogenetic analysis of combined data. Syst Biol 53:47–67. doi: 10.1080/10635150490264699 PubMedGoogle Scholar
  104. O’Brien TG, Kinnaird MF, Dierenfeld ES et al (1998) Gene translocation links insects and crustaceans. Nature 392:667–668. doi: 10.1038/33580 Google Scholar
  105. Ometto L, Stephan W, De Lorenzo D (2005) Insertion/deletion and nucleotide polymorphism data reveal constraints in Drosophila melanogaster introns and intergenic regions. Genetics 169:1521–1527. doi: 10.1534/genetics.104.037689 PubMedGoogle Scholar
  106. Osada N, Wu C-I (2005) Inferring the mode of speciation from genomic data: a study of the great apes. Genetics 169:259–264. doi: 10.1534/genetics.104.029231 PubMedGoogle Scholar
  107. Otto SP, Cummings MP, Wakeley J (1996) Inferring phylogenies from DNA sequence data: the effects of sampling. In: Harvey PH, Leigh Brown AJ, Maynard Smith J, Nee S (eds) New uses for new phylogenies. Oxford University Press, New York, pp 103–115Google Scholar
  108. Page R, Charleston M (1997) From gene to organismal phylogeny: reconciled trees and the gene tree/species tree problem. Mol Phyl Evol 7:231–240. doi: 10.1006/mpev.1996.0390 Google Scholar
  109. Palumbi SR (1996) The polymerase chain reaction. In: DM Hillis, Moritz C, Mable BK (eds) Molecular systematics. Sinauer Associates, Inc, pp 205–247Google Scholar
  110. Palumbi S, Baker C (1994) Contrasting population structure from nuclear intron sequences and mtDNA of Humpback whales. Mol Biol Evol 11:426–435PubMedGoogle Scholar
  111. Pamilo P, Nei M (1988) Relationships between gene trees and species trees. Mol Biol Evol 5:568–583PubMedGoogle Scholar
  112. Patterson N, Richter DJ, Gnerre S, Lander ES, Reich D (2006) Genetic evidence for complex speciation of humans and chimpanzees. Nature 441:1103–1108. doi: 10.1038/nature04789 PubMedGoogle Scholar
  113. Peters JL, Zhuravlev Y, Fefelov I, Logie A, Omland KE (2007) Nuclear loci and coalescent methods support ancient hybridization as cause of mitochondrial paraphyly between gadwall and falcated duck (Anas spp.). Evol Int J Org Evol 61:1992–2006. doi: 10.1111/j.1558-5646.2007.00149.x Google Scholar
  114. Pluzhnikov A, Donnelly P (1996) Optimal sequencing strategies for surveying molecular genetic diversity. Genetics 144:1247–1262PubMedGoogle Scholar
  115. Pluzhnikov A, Rienzo AD, Hudson RR (2002) Inferences about human demography based on multilocus analyses of noncoding sequences. Genetics 161:1209–1218PubMedGoogle Scholar
  116. Pollard DA, Iyer VN, Moses AM, Eisen MB (2006) Widespread discordance of gene trees with species tree in Drosophila: evidence for incomplete lineage sorting. PLoS Genet 2:e173. doi: 10.1371/journal.pgen.0020173
  117. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  118. Rokas A, Carroll SB (2006) Bushes in the tree of life. PLoS Biol 4:1899–1904. doi: 10.1371/journal.pbio.0040352 Google Scholar
  119. Rokas A, Holland PWH (2000) Rare genomic changes as a tool for phylogenetics. Trends Ecol Evol 15:454–459. doi: 10.1016/S0169-5347(00)01967-4 PubMedGoogle Scholar
  120. Rokas A, Williams BL, King N, Carroll SB (2003) Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425:798–804. doi: 10.1038/nature02053 PubMedGoogle Scholar
  121. Rokas A, Krüger D, Carroll SB (2005) Animal evolution and the molecular signature of radiations compressed in time. Science 310:1933–1938. doi: 10.1126/science.1116759 PubMedGoogle Scholar
  122. Rosenblum EB, Novembre J (2007) Ascertainment bias in spatially structured populations: a case study in the eastern fence lizard. J Hered 98:331–336. doi: 10.1093/jhered/esm031 PubMedGoogle Scholar
  123. Rosenblum EB, Hickerson MJ, Moritz C (2007) A multilocus perspective on colonization accompanied by selection and gene flow. Evol Int J Org Evol 61:2971–2985. doi: 10.1111/j.1558-5646.2007.00251.x Google Scholar
  124. Ross CL, Harrison RG (2002) A fine-scale spatial analysis of the mosaic hybrid zone between Gryllus firmus and Grillus pennsylvanicus. Evol Int J Org Evol 56:2296–2312Google Scholar
  125. Rubinsztein DC, Amos B, Cooper G (1999) Microsatellite and trinucleotide-repeat evolution: evidence for mutational bias and different rates of evolution in different lineages. Philos Trans R Soc Lond B Biol Sci 354:1095–1099. doi: 10.1098/rstb.1999.0465 PubMedGoogle Scholar
  126. Seo T-K, Kishino H, Thorne JT (2005) Incorporating gene-specific variation when inferring and evaluating optimal evolutionary tree topologies from multilocus sequence data. Proc Natl Acad Sci (USA) 102:4436–4441Google Scholar
  127. Shaffer HB, Thomson RC (2007) Delimiting species in recent radiations. Syst Biol 56:896–906. doi: 10.1080/10635150701772563 PubMedGoogle Scholar
  128. Shedlock AM, Milinkovitch MC, Okada N (2000) SINE evolution, missing data, and the origin of whales. Syst Biol 49:808–817. doi: 10.1080/106351500750049851 PubMedGoogle Scholar
  129. Shedlock AM, Takahashi K, Okada N (2004) SINEs of speciation: tracking lineages with retroposons. Trends Ecol Evol 19:545–553. doi: 10.1016/j.tree.2004.08.002 PubMedGoogle Scholar
  130. Shriver MD, Kennedy GC, Parra EJ et al (2004) The genomic distribution of population substructure in four populations using 8, 525 autosomal SNPs. Hum Genomics 1:274–286PubMedGoogle Scholar
  131. Shriver MD, Mei R, Parra EJ et al (2005) Large-scale SNP analysis reveals clustered and continuous patterns of human genetic variation. Hum Genomics 2:81–89PubMedGoogle Scholar
  132. Sites JW Jr, Marshall JC (2003) Delimiting species: a renaissance issue in systematic biology. Trends Ecol Evol 18:462–470. doi: 10.1016/S0169-5347(03)00184-8 Google Scholar
  133. Sites JW Jr, Marshall JC (2004) Operational criteria for delimiting species. Annu Rev Ecol Syst 35:199–227. doi: 10.1146/annurev.ecolsys.35.112202.130128 Google Scholar
  134. Slatkin M, Maddison WP (1989) A cladistic measure of gene flow inferred from the phylogenies of alleles. Genetics 123:603–613PubMedGoogle Scholar
  135. Small KS, Brudno M, Hill MM, Sidow A (2007) Extreme genomic variation in a natural population. Proc Natl Acad Sci USA 104:5698–5703. doi: 10.1073/pnas.0700890104 PubMedGoogle Scholar
  136. Stephens M, Smith N, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989. doi: 10.1086/319501 PubMedGoogle Scholar
  137. Storz JF (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol Ecol 14:671–688. doi: 10.1111/j.1365-294X.2005.02437.x PubMedGoogle Scholar
  138. 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. doi: 10.1093/molbev/msh192 PubMedGoogle Scholar
  139. Takahata N (1989) Gene genealogy in three related populations: consistency probability between gene and population trees. Genetics 122:957–966PubMedGoogle Scholar
  140. Tautz D (1989) Hypervariability of simple sequences as a general source for polymorphic DNA markers. Nucleic Acids Res 17:6463–6471. doi: 10.1093/nar/17.16.6463 PubMedGoogle Scholar
  141. Templeton AR (1998) Nested clades analyses of phylogeographic data: testing hypotheses about gene flow and population history. Genetics 7:381–397Google Scholar
  142. Teshima KM, Coop G, Przeworski M (2006) How reliable are empirical genomic scans for selective sweeps? Genome Res 16:702–712. doi: 10.1101/gr.5105206 PubMedGoogle Scholar
  143. Thalmann O, Fischer A, Lankester F, Pääbo S, Vigilant L (2006) The complex evolutionary history of gorillas: insights from genomic data. Mol Biol Evol 24:146–158. doi: 10.1093/molbev/msl160 PubMedGoogle Scholar
  144. Tosi AJ, Morales JC, Melnick DJ (2003) Paternal, maternal, and biparental molecular markers provide unique windows onto the evolutionary history of macaque monkeys. Evol Int J Org Evol 57:1419–1435Google Scholar
  145. Townsend AK, Rimmer CC, Latta SC, Lovette IJ (2007) Ancient differentiation in the single-island avian radiation of endemic Hispaniolan chat-tanagers (Aves: Calyptophilus). Mol Ecol 16:3634–3642. doi: 10.1111/j.1365-294X.2007.03422.x PubMedGoogle Scholar
  146. Väli Ü, Brandström M, Johansson M, Ellegren H (2008) Insertion-deletion polymorphisms (indels) as genetic markers in natural populations. BMC Genet 9:8Google Scholar
  147. Vera JC, Wheat CW, Fescemyer HW et al (2008) Rapid transcriptome characterization for a nonmodel organism using 454 pyrosequencing. Mol Ecol 17:1636–1647. doi: 10.1111/j.1365-294X.2008.03666.x PubMedGoogle Scholar
  148. Voight BF, Adams AM, Frisse LA et al (2005) Interrogating multiple aspects of variation in a full resequencing data set to infer human population size changes. Proc Natl Acad Sci USA 102:18508–18513. doi: 10.1073/pnas.0507325102 PubMedGoogle Scholar
  149. Waddell PJ (2002) Very fast algorithms for evaluating the stability of ML and Bayesian phylogenetic trees from sequence data. Genome Inform 13:82–92Google Scholar
  150. Waddell PJ, Kishino H, Ota R (2001) A phylogenetic foundation for comparative mammalian genomics. Genome Inform 12:141–154PubMedGoogle Scholar
  151. Wakeley J (2002) Inferences about the structure and history of populations: coalescents and intraspecific phylogeography. In: Singh R, Uyenoyama M, Jain S (eds) The evolution of population biology—Modern synthesis. Cambridge University Press, CambridgeGoogle Scholar
  152. Wakeley J (2004) Recent trends in population genetics: more data! more math! simple models? J Hered 95:397–405. doi: 10.1093/jhered/esh062 PubMedGoogle Scholar
  153. Wang R, Wakeley J, Hey J (1997) Gene flow and natural selection in the origin of Drosophila pseudoobscura and close relatives. Genetics 147:1091–1106PubMedGoogle Scholar
  154. Watterson GA (1978) The homozygosity test of neutrality. Genetics 88:405–417PubMedGoogle Scholar
  155. Whitfield CW, Behura SK, Berlocher SH et al (2006) Thrice out of Africa: ancient and recent expansions of the honey bee, Apis mellifera. Science 314:642–645. doi: 10.1126/science.1132772 PubMedGoogle Scholar
  156. Wilder JA, Kingan SB, Mobasher Z, Pilkington MM, Hammer MF (2004) Global patterns of human mitochondrial DNA and Y-chromosome structure are not influenced by higher migration rates of females versus males. Nat Genet 36:1122–1125. doi: 10.1038/ng1428 PubMedGoogle Scholar
  157. Wilson AC, Cann RL, Carr SM et al (1985) Mitochondrial DNA and two perspectives on evolutionary genetics. Biol J Linn Soc 26:375–400. doi: 10.1111/j.1095-8312.1985.tb02048.x Google Scholar
  158. Wolfe KH, Li W-H, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci USA 84:9054–9058. doi: 10.1073/pnas.84.24.9054 PubMedGoogle Scholar
  159. Wu CI (1991) Inferences of species phylogeny in relation to segregation of ancient polymorphisms. Genetics 127:429–435PubMedGoogle Scholar
  160. Zhang D-X, Hewitt GM (2003) Nuclear DNA analyses in genetic studies of populations: practice, problems and prospects. Mol Ecol 12:563–584. doi: 10.1046/j.1365-294X.2003.01773.x PubMedGoogle Scholar
  161. Zink RM, Barrowclough GF (2008) Mitochondrial DNA under siege in avian phylogeography. Mol Ecol 17:2107–2121. doi: 10.1111/j.1365-294X.2008.03737.x PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  1. 1.Department of Organismic and Evolutionary BiologyHarvard UniversityCambridge USA
  2. 2.Instituto Gulbenkian de CiênciaOeirasPortugal

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