Bears in a forest of gene trees: Phylogenetic inference is complicated by incomplete lineage sorting and gene flow

Molecular Biology and Evolution

Volumn 31, Issue 8, 2014, Pages 2004-2017

  Kutschera, Verena E ^a   Bidon, Tobias ^a   Hailer, Frank ^a   Rodi, Julia L ^a   Fain, Steven R ^b   Janke, Axel ^a,c  

^a BIODIVERSITY AND CLIMATE RESEARCH CENTRE BIK F   (Germany)

^b US Fish and Wildlife National Forensics Laboratory   (United States)

^c GOETHE UNIVERSITY   (Germany)

Author keywords

coalescence; introgressive hybridization; multi locus analyses; phylogenetic network; species tree; Ursidae

Indexed keywords

CELL NUCLEUS DNA; MITOCHONDRIAL DNA;

ALLELE; ARTICLE; ASIAN BLACK BEAR; BEAR; BLACK BEAR; BROWN BEAR; FEMALE; GENE FLOW; GENE LOCUS; GENE TREE DISCORDANCE; GENEALOGY; GENETIC VARIABILITY; INCOMPLETE LINEAGE SORTING; INTERSPECIFIC HYBRIDIZATION; INTROGRESSION; INTRON; MALE; MARKER GENE; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; NONHUMAN; PHYLOGENETIC INCONGRUENCE; PHYLOGENETIC INFERENCE; PHYLOGENETIC TREE; SLOTH BEAR; SPECIES DIFFERENCE; Y CHROMOSOME; ANIMAL; CELL NUCLEUS; CLASSIFICATION; DNA SEQUENCE; GENETICS; MITOCHONDRION; PHYLOGENY; PROCEDURES; SPECIES DIFFERENTIATION;

ANIMALS; CELL NUCLEUS; EVOLUTION, MOLECULAR; GENE FLOW; GENETIC SPECIATION; INTRONS; MALE; MITOCHONDRIA; PHYLOGENY; SEQUENCE ANALYSIS, DNA; URSIDAE; Y CHROMOSOME;

EID: 84904966117     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msu186     Document Type: Article

References (93)

1. Abella J, Alba DM, Robles JM, Valenciano A, Rotgers C, Carmona R, Montoya P, Morales J. 2012. Kretzoiarctos gen. nov. , the oldest member of the giant panDa clade. PLoS One 7:e48985
2. Bapteste E, Van Iersel L, Janke A, Kelchner S, Kelk S, McInerney JO, Morrison DA, Nakhleh L, Steel M, Stougie L, et al. 2013. Networks: Expanding evolutionary thinking. Trends Genet. 29:439-441
3. Bidon T, Janke A, Fain SR, Eiken HG, Hagen SB, Saarma U, Hallström BM, Lecomte N, Hailer F. 2014. Brown and polar bear Y chromosomes reveal extensive male-biased gene flow within brother lineages. Mol Biol Evol. 31:1353-1363
4. Bonner JT. 1965. Size and cycles: An essay on the structure of biology. Princeton (NY): Princeton University Press
5. Bouckaert RR. 2010. DensiTree: Making sense of sets of phylogenetic trees. Bioinformatics 26:1372-1373
6. Cahill JA, Green RE, Fulton TL, Stiller M, Jay F, Ovsyanikov N, Salamzade R, St. John J, Stirling I, Slatkin M, et al. 2013. Genomic evidence for island population conversion resolves conflicting theories of polar bear evolution. PLoS Genet. 9:e1003345
7. Chan KMA, Levin SA. 2005. Leaky prezygotic isolation and porous genomes: Rapid introgression of maternally inherited DNA. Evolution 59:720-729
8. Chan Y-C, Roos C, Inoue-Murayama M, Inoue E, Shih C-C, Pei KJ-C, Vigilant L. 2013. Inferring the evolutionary histories of divergences in Hylobates and Nomascus gibbons through multilocus sequence data. BMC Evol Biol. 13:82
9. Clement M, PosaDa D, Crandall KA. 2000. TCS: A computer program to estimate gene genealogies. Mol Ecol. 9:1657-1659
10. Cronin MA, Amstrup SC, Garner GW, Vyse ER. 1991. Interspecific and intraspecific mitochondrial DNA variation in North American bears (Ursus). Can J Zool. 69:2985-2992
11. Cronin MA, Amstrup SC, Talbot SL, Sage GK, Amstrup KS 2009. Genetic variation, relatedness, and effective population size of polar bears (Ursus maritimus) in the southern Beaufort Sea, Alaska. J Hered. 100: 681-690
12. Cronin MA, McDonough MM, Huynh HM, Baker RJ 2013. Genetic relationships of North American bears (Ursus) inferred fromamplified fragment length polymorphisms and mitochondrial DNA sequences. Can J Zool. 91:626-634
13. Crouse J, Amorese D. 1987. Ethanol precipitation: Ammonium acetate as an alternative to sodium acetate. Focus 19:13-16
14. Darwin CR. 1859. On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. London: John Murray
15. Dmitriev DA, Rakitov RA. 2008. Decoding of superimposed traces produced by direct sequencing of heterozygous indels. PLoS Comput Biol. 4:e1000113
16. Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M. 2012. Geneious v5. 6. [Internet]. [2012 Mar]. Available from: Http://www. geneious. com
17. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A. 2006. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4:e88
18. Drummond AJ, Suchard MA, Xie D, Rambaut A. 2012. Bayesian phylogenetics wit BEAUti and the BEAST 1. 7. Mol Biol Evol. 29: 1969-1973
19. Edwards CJ, Suchard MA, Lemey P, Welch JJ, Barnes I, Fulton TL, Barnett R, O'Connell TC, Coxon P, Monaghan N, et al. 2011. Ancient hybridization and an Irish origin for the modern polar bear matriline. Curr Biol. 21:1251-1258
20. Excoffier L, Lischer HEL. 2010. Arlequin suite ver 3. 5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour. 10:564-567
21. Flot J-F. 2007. champuru 1. 0: A computer software for unraveling mixtures of two DNA sequences of unequal lengths. Mol Ecol Notes. 7: 974-977
22. Fortelius M (coordinator). 2003. New and old worlds database of fossil mammals (NOW). University Helsinki. [cited 2014 Jan]. Available from: Http://www. helsinki. fi/science/now
23. 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
24. Garrick RC, Sunnucks P, Dyer RJ. 2010. Nuclear gene phylogeography using PHASE: Dealing with unresolved genotypes, lost alleles, and systematic bias in parameter estimation. BMC Evol Biol. 10:118
25. Good JM, Hird S, Reid N, Demboski JR, Steppan SJ, Martin-Nims TR, Sullivan J. 2008. Ancient hybridization and mitochondrial capture between two species of chipmunks. Mol Ecol. 17:1313-1327
26. Gray A. 1972. Mammalian hybrids. A check-list with bibliography. Slough (United Kingdom): Commonwealth Agricultural Bureaux
27. Hailer F, Kutschera VE, Hallström BM, Fain SR, Leonard JA, Arnason U, Janke A. 2013. Response to comment on "Nuclear genomic sequences reveal that polar bears are an old and distinct bear lineage". Science 339:1522
28. Hailer F, Kutschera VE, Hallström BM, Klassert D, Fain SR, Leonard JA, Arnason U, Janke A. 2012. Nuclear genomic sequences reveal that polar bears are an old and distinct bear lineage. Science 336: 344-347
29. Hallast P, Balaresque P, Bowden GR, Ballereau S, Jobling MA. 2013. Recombination dynamics of a human Y-chromosomal palindrome: Rapid GC-biased gene conversion, multi-kilobase conversion tracts, and rare inversions. PLoS Genet. 9:e1003666
30. Hallström BM, Janke A. 2010. Mammalian evolution may not be strictly bifurcating. Mol Biol Evol. 27:2804-2816
31. Harrigan RJ, Mazza ME, Sorenson MD. 2008. Computation vs. cloning: Evaluation of two methods for haplotype determination. Mol Ecol Resour. 8:1239-1248
32. Heled J, Drummond AJ. 2010. Bayesian inference of species trees from multilocus data. Mol Biol Evol. 27:570-580
33. Hellborg L, Ellegren H. 2004. Low levels of nucleotide diversity in mammalian Y chromosomes. Mol Biol Evol. 21:158-163
34. Hey J. 2010. Isolation with migration models for more than two populations. Mol Biol Evol. 27:905-920
35. 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
36. Hobolth A, Dutheil JY, Hawks J, Schierup MH, Mailund T. 2011. Incomplete lineage sorting patterns among human, chimpanzee, and orangutan suggest recent orangutan speciation and widespread selection. Genome Res. 21:349-356
37. Hoffecker JF, Elias SA. 2007. The human ecology of Beringia. New York: Columbia University Press
38. Holland BR, Huber KT, Moulton V, Lockhart PJ. 2004. Using consensus networks to visualize contradictory evidence for species phylogeny. Mol Biol Evol. 21:1459-1461
39. Huson DH, Bryant D. 2006. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol. 23:254-267
40. Jacobsen F, Omland KE. 2012. Extensive introgressive hybridization within the northern oriole group (Genus Icterus) revealed by three-species isolation with migration analysis. Ecol Evol. 2: 2413-2429
41. Jameson D, Gibson AP, Hudelot C, Higgs PG. 2003. OGRe: A relational database for comparative analysis of mitochondrial genomes. Nucleic Acids Res. 31:202-206
42. Jobb G, von Haeseler A, Strimmer K. 2004. TREEFINDER: A powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol. 4:18
43. Kass RE, Raftery AE. 1995. Bayes factors. J Am Stat Assoc. 90:773-795
44. Kelly BP, Whiteley A, Tallmon D. 2010. The Arctic melting pot. Nature 468:891
45. Krause J, Unger T, Nocon A, Malaspinas A-S, Kolokotronis S-O, Stiller M, Soibelzon L, Spriggs H, Dear PH, Briggs AW, et al. 2008. Mitochondrial genomes reveal an explosive radiation of extinct and extant bears near the Miocene-Pliocene boundary. BMC Evol Biol. 8:220
46. Kubatko LS, Degnan JH. 2007. Inconsistency of phylogenetic estimates from concatenated data under coalescence. Syst Biol. 56: 17-24
47. Kurtén B. 1968. Pleistocene mammals of Europe. Chicago (IL): Aldine
48. Kurtén B, Anderson E. 1980. Pleistocene mammals of North America. New York: Columbia University Press
49. Lanier HC, Knowles LL 2012. Is recombination a problem for speciestree analyses? Syst Biol. 61:691-701
50. Leaché AD, Harris RB, Rannala B, Yang Z. 2014. The influence of gene flow on species tree estimation: A simulation study. Syst Biol. 63: 17-30
51. Li R, Fan W, Tian G, Zhu H, He L, Cai J, Huang Q, Cai Q, Li B, Bai Y, et al. 2010. The sequence and De novo assembly of the giant panda genome. Nature 463:311-317
52. Librado P, Rozas J. 2009. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451-1452
53. Lischer HEL, Excoffier L, Heckel G. 2014. Ignoring heterozygous sites biases phylogenomic estimates of divergence times: Implications for the evolutionary history of Microtus voles. Mol Biol Evol. 31: 817-831
54. Liu S, Lorenzen ED, Fumagalli M, Li B, Harris K, Xiong Z, Zhou L, Korneliussen TS, Somel M, Babbitt C, et al. 2014. Population genomics reveal recent speciation and rapid evolutionary adaptation in polar bears. Cell 157:785-794
55. Maddison WP, Knowles LL. 2006. Inferring phylogeny despite incomplete lineage sorting. Syst Biol. 55:21-30
56. Mallet J. 2005. Hybridization as an invasion of the genome. Trends Ecol Evol. 20:229-237
57. McKay BD, Zink RM. 2010. The causes of mitochondrial DNA gene tree paraphyly in birds. Mol Phylogenet Evol. 54:647-650
58. Melo-Ferreira J, Boursot P, Carneiro M, Esteves PJ, Farelo L, Alves PC. 2012. Recurrent introgression of mitochondrial DNA among hares (Lepus spp. ) revealed by species-Tree inference and coalescent simulations. Syst Biol. 61:367-381
59. Miller W, Schuster SC, Welch AJ, Ratan A, Bedoya-Reina OC, Zhao F, Lim Kim H, Burhans RC, Drautz DI, Wittekindt NE, et al. 2012. Polar and brown bear genomes reveal ancient admixture and demographic footprints of past climate change. Proc Natl Acad Sci U S A. 109: E2382-E2390
60. Morrison DA. 2005. Networks in phylogenetic analysis: New tools for population biology. Int J Parasitol. 35:567-582
61. Nachman MW, Crowell SL. 2000. Estimate of the mutation rate per nucleotide in humans. Genetics 156:297-304
62. Nakagome S, Mano S, Hasegawa M. 2013. Comment on "Nuclear genomic sequences reveal that polar bears are an old and distinct bear lineage". Science 339:1522
63. Nakagome S, Pecon-Slattery J, MasuDa R. 2008. Unequal rates of Y chromosome gene divergence during speciation of the family Ursidae. Mol Biol Evol. 25:1344-1356
64. Nakhleh L. 2013. Computational approaches to species phylogeny inference and gene tree reconciliation. Trends Ecol Evol. 28: 719-728
65. Nichols R. 2001. Gene trees and species trees are not the same. Trends Ecol Evol. 16:358-364
66. Nielsen R, Wakeley J. 2001. Distinguishing migration from isolation: A Markov chain Monte Carlo approach. Genetics 158:885-896
67. Onorato DP, Hellgren EC, Bussche RA, Van D, Doan-Crider DL. 2004. Phylogeographic patterns within a metapopulation of black bears (Ursus americanus) in the American southwest. J Mammal. 85: 140-147
68. Pagès M, Bazin E, Galan M, Chaval Y, Claude J, Herbreteau V, Michaux J, Piry S, Morand S, Cosson J-F. 2013. Cytonuclear discordance among Southeast Asian black rats (Rattus rattus complex). Mol Ecol. 22: 1019-1034
69. Pagès M, Calvignac S, Klein C, Paris M, Hughes S, Hänni C. 2008. Combined analysis of fourteen nuclear genes refines the Ursidae phylogeny. Mol Phylogenet Evol. 47:73-83
70. Pamilo P, Nei M. 1988. Relationships between gene trees and species trees. Mol Biol Evol. 5:568-583
71. Petit E, Balloux F, Excoffier L. 2002. Mammalian population genetics: Why not Y? Trends Ecol Evol. 17:28-33
72. PosaDa D. 2008. jModelTest: Phylogenetic model averaging. Mol Biol Evol. 25:1253-1256
73. Prüfer K, Munch K, Hellmann I, Akagi K, Miller JR, Walenz B, Koren S, Sutton G, Kodira C, Winer R, et al. 2012. The bonobo genome compared with the chimpanzee and human genomes. Nature 486:527-531
74. Roca AL, Georgiadis N, O'Brien SJ. 2005. Cytonuclear genomic dissociation in African elephant species. Nat Genet. 37:96-100
75. Roos C, Zinner D, Kubatko LS, Schwarz C, Yang M, Meyer D, Nash SD, Xing J, Batzer MA, Brameier M, et al. 2011. Nuclear versus mitochondrial DNA: Evidence for hybridization in colobine monkeys. BMC Evol Biol. 11:77
76. Sachidanandam R, Weissman D, Schmidt SC, Kakol JM, Stein LD, Marth G, Sherry S, Mullikin JC, Mortimore BJ, Willey DL, et al. 2001. A map of human genome sequence variation containing 1. 42 million single nucleotide polymorphisms. Nature 409:928-933
77. Sambrook J, Russell DW. 2000. Molecular cloning: A laboratory manual. New York: Cold Spring Harbor Laboratory Press
78. Scally A, Dutheil JY, Hillier LW, Jordan GE, Goodhead I, Herrero J, Hobolth A, Lappalainen T, Mailund T, Marques-Bonet T, et al. 2012. Insights into hominid evolution from the gorilla genome sequence. Nature 483:169-175
79. Schwenk K, Brede N, Streit B. 2008. Introduction. Extent, processes and evolutionary impact of interspecific hybridization in animals. Philos Trans R Soc B Biol Sci. 363:2805-2811
80. Servheen C. 1990. The status and conservation of the bears of the world. Int Conf Bear Res and Manage Monogr Series 2:1-32
81. Shimodaira H. 2002. An approximately unbiased test of phylogenetic tree selection. Syst Biol. 51:492-508
82. Suchard MA, Weiss RE, Sinsheimer JS. 2005. Models for estimating Bayes factors with applications to phylogeny and tests of monophyly. Biometrics 61:665-673
83. Tajima F. 1983. Evolutionary relationship of Dna sequences in finite populations. Genetics 105:437-460
84. Tallmon DA, Bellemain E, Swenson JE, Taberlet P. 2004. Genetic monitoring of Scandinavian brown bear effective population size and immigration. J Wildl Manag. 68:960-965
85. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 28:2731-2739
86. Waddell PJ, Kishino H, Ota R. 2001. A phylogenetic foundation for comparative mammalian genomics. Genome Inform. 12:141-154
87. Wayne RK, Van Valkenburgh B, O'Brien SJ. 1991. Molecular distance and divergence time in carnivores and primates. Mol Biol Evol. 8: 297-319
88. Woerner AE, Cox MP, Hammer MF. 2007. Recombination-filtered genomic data sets by information maximization. Bioinformatics 23: 1851-1853
89. Yu L, Li Q-W, Ryder OA, Zhang Y-P. 2004. Phylogeny of the bears (Ursidae) based on nuclear and mitochondrial genes. Mol Phylogenet Evol. 32:480-494
90. Yu L, Li Y-W, Ryder OA, Zhang Y-P. 2007. Analysis of complete mitochondrial genome sequences increases phylogenetic resolution of bears (Ursidae), a mammalian family that experienced rapid speciation. BMC Evol Biol. 7:198
91. Yu Y, Barnett RM, Nakhleh L. 2013. Parsimonious inference of hybridization in the presence of incomplete lineage sorting. Syst Biol. 62: 738-751
92. Yu Y, Degnan JH, Nakhleh L. 2012. The probability of a gene tree topology within a phylogenetic network with applications to hybridization detection. PLoS Genet. 8:e1002660
93. Zhao S, Zheng P, Dong S, Zhan X, Wu Q, Guo X, Hu Y, He W, Zhang S, Fan W, et al. 2013. Whole-genome sequencing of giant pandas provides insights into demographic history and local adaptation. Nat Genet. 45:67-71.