Tandem duplications and the limits of natural selection in Drosophila yakuba and Drosophila simulans

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Rogers, Rebekah L ^a   Cridland, Julie M ^b   Shao, Ling ^c   Hu, Tina T ^d   Andolfatto, Peter ^d   Thornton, Kevin R ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CONTROLLED STUDY; DROSOPHILA SIMULANS; DROSOPHILA YAKUBA; EVOLUTIONARY ADAPTATION; FEMALE; GENE DUPLICATION; GENE IDENTIFICATION; GENE MUTATION; GENE ONTOLOGY; GENETIC CODE; GENETIC SELECTION; GENETIC VARIABILITY; NONHUMAN; PHENOTYPE; POPULATION GENETICS; POPULATION SIZE; SINGLE NUCLEOTIDE POLYMORPHISM; TANDEM REPEAT; X CHROMOSOME; ANIMAL; DROSOPHILA; EVOLUTION; GENETIC VARIATION; GENETICS; INSECT GENOME; STATISTICAL MODEL;

ANIMALS; BIOLOGICAL EVOLUTION; DROSOPHILA; DROSOPHILA SIMULANS; GENE DUPLICATION; GENETIC VARIATION; GENOME, INSECT; LIKELIHOOD FUNCTIONS; POLYMORPHISM, SINGLE NUCLEOTIDE; SELECTION, GENETIC; X CHROMOSOME;

EID: 84941342399     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0132184     Document Type: Article

References (96)

1. Conant GC, Wolfe KH. Turning a hobby into a job: how duplicated genes find new functions. Nat Rev Genet. 2008 Dec; 9(12):938-950. doi: 10.1038/nrg2482 PMID: 19015656
2. Ohno S. Evolution by gene duplication. London: George Alien & Unwin Ltd. Berlin, Heidelberg and New York: Springer-Verlag.; 1970.
3. Magwire MM, Bayer F, Webster CL, Cao C, Jiggins FM. Successive increases in the resistance of Drosophila to viral infection through a transposon insertion followed by a Duplication. PLoS Genet. 2011 Oct; 7(10):e1002337. doi: 10.1371/journal.pgen.1002337 PMID: 22028673
4. Rogers RL, Cridland JM, Shao L, Hu TT, Andolfatto P, Thornton KR. Landscape of Standing Variation for Tandem Duplications in Drosophila yakuba and Drosophila simulans. Mol Biol Evol. 2014 Jul; 31 (7):1750-1766. doi: 10.1093/molbev/msu124 PMID: 24710518
5. Emerson JJ, Cardoso-Moreira M, Borevitz JO, Long M. Natural selection shapes genome-wide patterns of copy-number polymorphism in Drosophila melanogaster. Science. 2008 Jun; 320(5883):1629-1631. doi: 10.1126/science.1158078 PMID: 18535209
6. Cardoso-Moreira M, Emerson JJ, Clark AG, Long M. Drosophila duplication hotspots are associated with late-replicating regions of the genome. PLoS Genet. 2011 Nov; 7(11):e1002340. doi: 10.1371/journal.pgen.1002340 PMID: 22072977
7. Dopman EB, Hartl DL. A portrait of copy-number polymorphism in Drosophila melanogaster. Proc Natl Acad Sci USA. 2007 Dec; 104(50):19920-19925. doi: 10.1073/pnas.0709888104 PMID: 18056801
8. Zhou Q, Zhang G, Zhang Y, Xu S, Zhao R, Zhan Z, et al. On the origin of new genes in Drosophila. Genome Research. 2008 Sep; 18(9):1446-1455. doi: 10.1101/gr.076588.108 PMID: 18550802
9. Katju V, Lynch M. On the formation of novel genes by duplication in the Caenorhabditis elegans genome. Molecular Biology and Evolution. 2006 May; 23(5):1056-1067. doi: 10.1093/molbev/msj114 PMID: 16500928
10. Rogers RL, Bedford T, Hartl DL. Formation and longevity of chimeric and duplicate genes in Drosophila melanogaster. Genetics. 2009 Jan; 181(1):313-322. doi: 10.1534/genetics.108.091538 PMID: 19015547
11. Hahn MW, Han MV, Han SG. Gene Family Evolution across 12 Drosophila Genomes. PLoS Genetics. 2007 Nov 9; 3(11):e197. doi: 10.1371/journal.pgen.0030197 PMID: 17997610
12. Rogers RL, Hartl DL. Chimeric genes as a source of rapid evolution in Drosophila melanogaster. Mol Biol Evol. 2012 Feb; 29(2):517-529. doi: 10.1093/molbev/msr184 PMID: 21771717
13. Jones CD, Begun DJ. Parallel evolution of chimeric fusion genes. Proceedings of the National Academy of Sciences, USA. 2005 Aug 9; 102(32):11373-11378. doi: 10.1073/pnas.0503528102
14. Shih HJ, Jones CD. Patterns of amino acid evolution in the Drosophila ananassae chimeric gene, siren, parallel those of other Adh-derived chimeras. Genetics. 2008 Oct; 180(2):1261-1263. doi: 10.1534/genetics.108.090068 PMID: 18780749
15. Long M, Langley CH. Natural selection and the origin of jingwei, a chimeric processed functional gene in Drosophila. Science. 1993 Apr 2; 260(5104):91-95. doi: 10.1126/science.7682012 PMID: 7682012
16. Zhang J, Dean AM, Brunet F, Long M. Evolving protein functional diversity in new genes of Drosophila. Proceedings of the National Academy of Sciences, USA. 2004 Nov 16; 101(46):16246-16250. doi: 10.1073/pnas.0407066101
17. Lynch M, Conery JS. The evolutionary fate and consequences of duplicate genes. Science. 2000 Nov; 290(5494):1151-1155. doi: 10.1126/science.290.5494.1151 PMID: 11073452
18. Hermisson J, Pennings PS. Soft sweeps: molecular population genetics of adaptation from standing genetic variation. Genetics. 2005 Apr; 169(4):2335-2352. doi: 10.1534/genetics.104.036947 PMID: 15716498
19. Maynard Smith J. What use is sex? Journal of theoretical biology. 1971; 30(2):319-335. doi: 10.1016/0022-5193(71)90058-0
20. Gillespie JH. 5. In: The Causes of Molecular Evolution. Oxford University Press; 1991. p. 232.
21. Kreitman M. Nucleotide polymorphism at the alcohol dehydrogenase locus of Drosophila melanogaster. Nature. 1983; 304(5925):412-417. doi: 10.1038/304412a0 PMID: 6410283
22. Bachtrog D, Thornton K, Clark A, Andolfatto P. Extensive introgression of mitochondrial DNA relative to nuclear genes in the Drosophila yakuba species group. Evolution. 2006 Feb; 60(2):292-302. doi: 10.1111/j.0014-3820.2006.tb01107.x PMID: 16610321
23. Andolfatto P, Wong KM, Bachtrog D. Effective population size and the efficacy of selection on the X chromosomes of two closely related Drosophila species. Genome Biol Evol. 2011; 3:114-128. doi: 10.1093/gbe/evq086 PMID: 21173424
24. Karasov T, Messer PW, Petrov DA. Evidence that adaptation in Drosophila is not limited by mutation at single sites. PLoS Genet. 2010 Jun; 6(6):e1000924. doi: 10.1371/journal.pgen.1000924 PMID: 20585551
25. Carneiro M, Hartl DL. Colloquium papers: Adaptive landscapes and protein evolution. Proceedings of the National Academy of Sciences, USA. 2010 Jan 26; 107 Suppl 1:1747-1751. doi: 10.1073/pnas. 0906192106
26. Cui Y, Wong WH, Bornberg-Bauer E, Chan HS. Recombinatoric exploration of novel folded structures: a heteropolymer-based model of protein evolutionary landscapes. Proceedings of the National Academy of Sciences, USA. 2002 Jan 22; 99(2):809-814. doi: 10.1073/pnas.022240299
27. Giver L, Arnold FH. Combinatorial protein design by in vitro recombination. Current Opinion in Chemical Biology. 1998 Jun; 2(3):335-338. doi: 10.1016/S1367-5931(98)80006-9 PMID: 9691067
28. Tamura K, Subramanian S, Kumar S. Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. Mol Biol Evol. 2004 Jan; 21(1):36-44. doi: 10.1093/molbev/msg236 PMID: 12949132
29. Gould SJ, Lewontin RC. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc R Soc Lond, B, Biol Sci. 1979 Sep; 205(1161):581-598. doi: 10.1098/rspb.1979.0086 PMID: 42062
30. Stern DL. The genetic causes of convergent evolution. Nat Rev Genet. 2013 Nov; 14(11):751-764. doi: 10.1038/nrg3483 PMID: 24105273
31. Chen L, DeVries AL, Cheng CH. Convergent evolution of antifreeze glycoproteins in Antarctic notothenioid fish and Arctic cod. Proc Natl Acad Sci USA. 1997 Apr; 94(8):3817-3822. doi: 10.1073/pnas.94.8. 3817 PMID: 9108061
32. Shapiro MD, Summers BR, Balabhadra S, Aldenhoven JT, Miller AL, Cunningham CB, et al. The genetic architecture of skeletal convergence and sex determination in ninespine sticklebacks. Curr Biol. 2009 Jul; 19(13):1140-1145. doi: 10.1016/j.cub.2009.05.029 PMID: 19500990
33. Brodie ED. Convergent evolution: pick your poison carefully. Curr Biol. 2010 Feb; 20(4):R152-154. doi: 10.1016/j.cub.2009.12.029 PMID: 20178758
34. Khadjeh S, Turetzek N, Pechmann M, Schwager EE, Wimmer EA, Damen WG, et al. Divergent role of the Hox gene Antennapedia in spiders is responsible for the convergent evolution of abdominal limb repression. Proc Natl Acad Sci USA. 2012 Mar; 109(13):4921-4926. doi: 10.1073/pnas.1116421109 PMID: 22421434
35. Wittkopp PJ, Williams BL, Selegue JE, Carroll SB. Drosophila pigmentation evolution: divergent genotypes underlying convergent phenotypes. Proc Natl Acad Sci USA. 2003 Feb; 100(4):1808-1813. doi: 10.1073/pnas.0336368100 PMID: 12574518
36. Tanaka K, Barmina O, Kopp A. Distinct developmental mechanisms underlie the evolutionary diversification of Drosophila sex combs. Proc Natl Acad Sci USA. 2009 Mar; 106(12):4764-4769. doi: 10.1073/pnas.0807875106 PMID: 19255422
37. Zhen Y, Aardema ML, Medina EM, Schumer M, Andolfatto P. Parallel molecular evolution in an herbivore community. Science. 2012 Sep; 337(6102):1634-1637. doi: 10.1126/science.1226630 PMID: 23019645
38. Riehle MM, Bennett AF, Long AD. Genetic architecture of thermal adaptation in Escherichia coli. Proc Natl Acad Sci USA. 2001 Jan; 98(2):525-530. doi: 10.1073/pnas.98.2.525 PMID: 11149947
39. Chan YF, Marks ME, Jones FC, Villarreal G, Shapiro MD, Brady SD, et al. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science. 2010 Jan; 327(5963):302-305. doi: 10.1126/science.1182213 PMID: 20007865
40. Moxon E, Lenski R, Rainey P. Adaptive evolution of highly mutable loci in pathogenic bacteria. Perspectives in Biology and Medicine. 1998; 42(1):154-155. doi: 10.1353/pbm.1998.0062 PMID: 10766604
41. Burke MK, Dunham JP, Shahrestani P, Thornton KR, Rose MR, Long AD. Genome-wide analysis of a long-term evolution experiment with Drosophila. Nature. 2010 Sep; 467(7315):587-590. doi: 10.1038/nature09352 PMID: 20844486
42. Woods R, Schneider D, Winkworth CL, Riley MA, Lenski RE. Tests of parallel molecular evolution in a long-term experiment with Escherichia coli. Proceedings of the National Academy of Sciences. 2006; 103(24):9107-9112. doi: 10.1073/pnas.0602917103
43. Tenaillon O, Rodriguez-Verdugo A, Gaut RL, McDonald P, Bennett AF, Long AD, et al. The molecular diversity of adaptive convergence. Science. 2012 Jan; 335(6067):457-461. doi: 10.1126/science. 1212986 PMID: 22282810
44. Orozco-terWengel P, Kapun M, Nolte V, Kofler R, Flatt T, Schloetterer C. Adaptation of Drosophila to a novel laboratory environment reveals temporally heterogeneous trajectories of selected alleles. Molecular ecology. 2012; 21(20):4931-4941. doi: 10.1111/j.1365-294X.2012.05673.x PMID: 22726122
45. Colosimo PF, Hosemann KE, Balabhadra S, Villarreal G, Dickson M, Grimwood J, et al. Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science. 2005 Mar; 307 (5717):1928-1933. doi: 10.1126/science.1107239 PMID: 15790847
46. Martin A, Papa R, Nadeau NJ, Hill RI, Counterman BA, Halder G, et al. Diversification of complex butterfly wing patterns by repeated regulatory evolution of a Wnt ligand. Proc Natl Acad Sci USA. 2012 Jul; 109(31):12632-12637. doi: 10.1073/pnas.1204800109 PMID: 22802635
47. Reinhardt JA, Kolaczkowski B, Jones CD, Begun DJ, Kern AD. Parallel geographic variation in Drosophila melanogaster. Genetics. 2014 May; 197(1):361-373. doi: 10.1534/genetics.114.161463 PMID: 24610860
48. Nielsen R, Bustamante C, Clark AG, Glanowski S, Sackton TB, Hubisz MJ, et al. A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol. 2005 Jun; 3(6):e170. doi: 10.1371/journal.pbio.0030170 PMID: 15869325
49. Tajima F. Evolutionary relationship of DNA sequences in finite populations. Genetics. 1983 Oct; 105 (2):437-460. PMID: 6628982
50. Watterson GA. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 1975 Apr; 7(2):256-276. doi: 10.1016/0040-5809(75)90020-9 PMID: 1145509
51. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989 Nov; 123(3):585-595. PMID: 2513255
52. Coop G, Ralph P. Patterns of neutral diversity under general models of selective sweeps. Genetics. 2012 Sep; 192(1):205-224. doi: 10.1534/genetics.112.141861 PMID: 22714413
53. Lemeunier F, Ashburner MA. Relationships within the melanogaster species subgroup of the genus Drosophila (Sophophora). II. Phylogenetic relationships between six species based upon polytene chromosome banding sequences. Proc R Soc Lond, B, Biol Sci. 1976 May; 193(1112):275-294. doi: 10.1098/rspb.1976.0046 PMID: 6967
54. Llopart A, Lachaise D, Coyne JA. Multilocus analysis of introgression between two sympatric sister species of Drosophila: Drosophila yakuba and D. santomea. Genetics. 2005 Sep; 171(1):197-210. doi: 10.1534/genetics.104.033597 PMID: 15965264
55. Mackay TF, Richards S, Stone EA, Barbadilla A, Ayroles JF, Zhu D, et al. The Drosophila melanogaster Genetic Reference Panel. Nature. 2012 Feb; 482(7384):173-178. doi: 10.1038/nature10811 PMID: 22318601
56. Cridland JM, Thornton KR. Validation of rearrangement break points identified by paired-end sequencing in natural populations of Drosophila melanogaster. Genome Biol Evol. 2010; 2:83-101. doi: 10.1093/gbe/evq001 PMID: 20333226
57. Chao A. Nonparametric estimation of the number of classes in a population. Scandinavian Journal of statistics. 1984;p. 265-270.
58. Hartl DL, Clark AG. In: Principles of population genetics. Sunderland, Mass.: Sinauer Associates; 2007. p. 652. Available from: http://www.loc.gov/catdir/toc/ecip074/2006036153.html.
59. Lynch M. In: The Origins of Genome Architecture. Sunderland, Mass.: Sinauer Associates; 2007. p. 494. Available from: http://www.loc.gov/catdir/toc/ecip077/2007000012.html.
60. Haldane JBS. A mathematical theory of natural and artificial selection V: Selection and Mutation. Proceedings of the Cambridge Philosophical Society. 1927; 23:838-844. doi: 10.1017/S0305004100011750
61. Jensen JD, Thornton KR, Andolfatto P. An approximate bayesian estimator suggests strong, recurrent selective sweeps in Drosophila. PLoS Genet. 2008; 4(9):e1000198. doi: 10.1371/journal.pgen. 1000198 PMID: 18802463
62. Andolfatto P. Hitchhiking effects of recurrent beneficial amino acid substitutions in the Drosophila melanogaster genome. Genome Res. 2007 Dec; 17(12):1755-1762. doi: 10.1101/gr.6691007 PMID: 17989248
63. Hu TT, Eisen MB, Thornton KR, Andolfatto P. A second-generation assembly of the Drosophila simulans genome provides new insights into patterns of lineage-specific divergence. Genome Res. 2013 Jan; 23(1):89-98. doi: 10.1101/gr.141689.112 PMID: 22936249
64. Zichner T, Garfield DA, Rausch T, Stutz AM, Cannavo E, Braun M, et al. Impact of genomic structural variation in Drosophila melanogaster based on population-scale sequencing. Genome Res. 2013 Mar; 23(3):568-579. doi: 10.1101/gr.142646.112 PMID: 23222910
65. Claycomb JM, Orr-Weaver TL. Developmental gene amplification: insights into DNA replication and gene expression. Trends Genet. 2005 Mar; 21(3):149-162. doi: 10.1016/j.tig.2005.01.009 PMID: 15734574
66. Charlesworth B, Morgan MT, Charlesworth D. The effect of deleterious mutations on neutral molecular variation. Genetics. 1993 Aug; 134(4):1289-1303. PMID: 8375663
67. Smith JM, Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Dec; 89(5-6):391-403.
68. Presgraves DC. Sex chromosomes and speciation in Drosophila. Trends Genet. 2008 Jul; 24(7):336-343. doi: 10.1016/j.tig.2008.04.007 PMID: 18514967
69. Thornton K, Long M. Rapid divergence of gene duplicates on the Drosophila melanogaster X chromosome. Mol Biol Evol. 2002 Jun; 19(6):918-925. doi: 10.1093/oxfordjournals.molbev.a004149 PMID: 12032248
70. Thornton K, Long M. Excess of amino acid substitutions relative to polymorphism between X-linked duplications in Drosophila melanogaster. Mol Biol Evol. 2005 Feb; 22(2):273-284. doi: 10.1093/molbev/msi015 PMID: 15483321
71. Lynch M, Conery JS. The evolutionary demography of duplicate genes. Journal of Structural and Functional Genomics. 2003; 3(1-4):35-44. doi: 10.1023/A:1022696612931 PMID: 12836683
72. Eyre-Walker A, Keightley PD, Smith NG, Gaffney D. Quantifying the slightly deleterious mutation model of molecular evolution. Mol Biol Evol. 2002 Dec; 19(12):2142-2149. doi: 10.1093/oxfordjournals. molbev.a004039 PMID: 12446806
73. Zhang YE, Vibranovski MD, Krinsky BH, Long M. Age-dependent chromosomal distribution of malebiased genes in Drosophila. Genome Res. 2010 Nov; 20(11):1526-1533. doi: 10.1101/gr.107334.110 PMID: 20798392
74. Bhutkar A, Schaeffer SW, Russo SM, Xu M, Smith TF, Gelbart WM. Chromosomal rearrangement inferred from comparisons of 12 Drosophila genomes. Genetics. 2008 Jul; 179(3):1657-1680. doi: 10.1534/genetics.107.086108 PMID: 18622036
75. Drosophila Twelve Genomes Consortium. Evolution of genes and genomes on the Drosophila phylogeny. Nature. 2007 Nov 8; 450(7167):203-218. doi: 10.1038/nature06341 PMID: 17994087
76. Lazarro BP, Clark AG. Rapid evolution of innate immune response genes. In: R S Singh JX, Kulathinal RJ, editors. Rapidly Evolving Genes and Genetic Systems. Oxford: Oxford University Press; 2012.
77. Beckerman AP, de Roij J, Dennis SR, Little TJ. A shared mechanism of defense against predators and parasites: chitin regulation and its implications for life-history theory. Ecol Evol. 2013 Dec; 3(15):5119-5126. doi: 10.1002/ece3.766 PMID: 24455141
78. Ffrench-Constant RH, Daborn PJ, Le Goff G. The genetics and genomics of insecticide resistance. Trends Genet. 2004 Mar; 20(3):163-170. doi: 10.1016/j.tig.2004.01.003 PMID: 15036810
79. Panhuis TM, Clark NL, Swanson WJ. Rapid evolution of reproductive proteins in abalone and Drosophila. Philos Trans R Soc Lond, B, Biol Sci. 2006 Feb; 361(1466):261-268. doi: 10.1098/rstb.2005.1793 PMID: 16612885
80. Begun DJ, Holloway AK, Stevens K, Hillier LW, Poh YP, Hahn MW, et al. Population genomics: wholegenome analysis of polymorphism and divergence in Drosophila simulans. PLoS Biol. 2007 Nov; 5(11): e310. doi: 10.1371/journal.pbio.0050310 PMID: 17988176
81. Schmidt JM, Good RT, Appleton B, Sherrard J, Raymant GC, Bogwitz MR, et al. Copy number variation and transposable elements feature in recent, ongoing adaptation at the Cyp6g1 locus. PLoS Genet. 2010 Jun; 6(6):e1000998. doi: 10.1371/journal.pgen.1000998 PMID: 20585622
82. Van Valen L. A new evolutionary law. Evolutionary theory. 1973; 1:1-30.
83. Bass C, Field LM. Gene amplification and insecticide resistance. Pest Manag Sci. 2011 Aug; 67 (8):886-890. doi: 10.1002/ps.2189 PMID: 21538802
84. Haddrill PR, Bachtrog D, Andolfatto P. Positive and negative selection on noncoding DNA in Drosophila simulans. Mol Biol Evol. 2008 Sep; 25(9):1825-1834. doi: 10.1093/molbev/msn125 PMID: 18515263
85. Andolfatto P, Wong KM, Bachtrog D. Effective population size and the efficacy of selection on the X chromosomes of two closely related Drosophila species. Genome Biol Evol. 2011; 3:114-128. doi: 10.1093/gbe/evq086 PMID: 21173424
86. Kaplan NL, Hudson RR, Langley CH. The "hitchhiking effect" revisited. Genetics. 1989 Dec; 123 (4):887-899. PMID: 2612899
87. Wakeley J. In: Coalescent Theory: An Introduction. Roberts & Company Publishers; 2009. p. 97.
88. Ewens WJ. A note on the sampling theory for infinite alleles and infinite sites models. Theor Popul Biol. 1974 Oct; 6(2):143-148. doi: 10.1016/0040-5809(74)90020-3 PMID: 4445971
89. Halligan DL, Keightley PD. Ubiquitous selective constraints in the Drosophila genome revealed by a genome-wide interspecies comparison. Genome Res. 2006 Jul; 16(7):875-884. doi: 10.1101/gr. 5022906 PMID: 16751341
90. Parsch J, Novozhilov S, Saminadin-Peter SS, Wong KM, Andolfatto P. On the utility of short intron sequences as a reference for the detection of positive and negative selection in Drosophila. Mol Biol Evol. 2010 Jun; 27(6):1226-1234. doi: 10.1093/molbev/msq046 PMID: 20150340
91. Clemente F, Vogl C. Unconstrained evolution in short introns?-an analysis of genome-wide polymorphism and divergence data from Drosophila. J Evol Biol. 2012 Oct; 25(10):1975-1990. doi: 10.1111/j. 1420-9101.2012.02580.x PMID: 22901008
92. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010 Sep; 20(9):1297-1303. doi: 10.1101/gr.107524.110 PMID: 20644199
93. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009 Aug; 25(16):2078-2079. doi: 10.1093/bioinformatics/btp352 PMID: 19505943
94. Thornton K. libsequence: a C++ class library for evolutionary genetic analysis. Bioinformatics. 2003; 19:2325-2327. doi: 10.1093/bioinformatics/btg316 PMID: 14630667
95. Haag-Liautard C, Dorris M, Maside X, Macaskill S, Halligan DL, Houle D, et al. Direct estimation of per nucleotide and genomic deleterious mutation rates in Drosophila. Nature. 2007 Jan 4; 445(7123):82-85. doi: 10.1038/nature05388 PMID: 17203060
96. Rosenberg NA. The shapes of neutral gene genealogies in two species: probabilities of monophyly, paraphyly, and polyphyly in a coalescent model. Evolution. 2003 Jul; 57(7):1465-1477. doi: 10.1554/03-012 PMID: 12940352