Recombinant Inbred Line Genotypes Reveal Inter-Strain Incompatibility and the Evolution of Recombination
The nematode Caenorhabditis briggsae is an emerging model organism that allows evolutionary comparisons with C. elegans and exploration of its own unique biological attributes. To produce a high-resolution C. briggsae recombination map, recombinant inbred lines were generated from reciprocal crosses between two strains and genotyped at over 1,000 loci. A second set of recombinant inbred lines involving a third strain was also genotyped at lower resolution. The resulting recombination maps exhibit discrete domains of high and low recombination, as in C. elegans, indicating these are a general feature of Caenorhabditis species. The proportion of a chromosome's physical size occupied by the central, low-recombination domain is highly correlated between species. However, the C. briggsae intra-species comparison reveals striking variation in the distribution of recombination between domains. Hybrid lines made with the more divergent pair of strains also exhibit pervasive marker transmission ratio distortion, evidence of selection acting on hybrid genotypes. The strongest effect, on chromosome III, is explained by a developmental delay phenotype exhibited by some hybrid F2 animals. In addition, on chromosomes IV and V, cross direction-specific biases towards one parental genotype suggest the existence of cytonuclear epistatic interactions. These interactions are discussed in relation to surprising mitochondrial genome polymorphism in C. briggsae, evidence that the two strains diverged in allopatry, the potential for local adaptation, and the evolution of Dobzhansky-Muller incompatibilities. The genetic and genomic resources resulting from this work will support future efforts to understand inter-strain divergence as well as facilitate studies of gene function, natural variation, and the evolution of recombination in Caenorhabditis nematodes.
Vyšlo v časopise:
Recombinant Inbred Line Genotypes Reveal Inter-Strain Incompatibility and the Evolution of Recombination. PLoS Genet 7(7): e32767. doi:10.1371/journal.pgen.1002174
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002174
Souhrn
The nematode Caenorhabditis briggsae is an emerging model organism that allows evolutionary comparisons with C. elegans and exploration of its own unique biological attributes. To produce a high-resolution C. briggsae recombination map, recombinant inbred lines were generated from reciprocal crosses between two strains and genotyped at over 1,000 loci. A second set of recombinant inbred lines involving a third strain was also genotyped at lower resolution. The resulting recombination maps exhibit discrete domains of high and low recombination, as in C. elegans, indicating these are a general feature of Caenorhabditis species. The proportion of a chromosome's physical size occupied by the central, low-recombination domain is highly correlated between species. However, the C. briggsae intra-species comparison reveals striking variation in the distribution of recombination between domains. Hybrid lines made with the more divergent pair of strains also exhibit pervasive marker transmission ratio distortion, evidence of selection acting on hybrid genotypes. The strongest effect, on chromosome III, is explained by a developmental delay phenotype exhibited by some hybrid F2 animals. In addition, on chromosomes IV and V, cross direction-specific biases towards one parental genotype suggest the existence of cytonuclear epistatic interactions. These interactions are discussed in relation to surprising mitochondrial genome polymorphism in C. briggsae, evidence that the two strains diverged in allopatry, the potential for local adaptation, and the evolution of Dobzhansky-Muller incompatibilities. The genetic and genomic resources resulting from this work will support future efforts to understand inter-strain divergence as well as facilitate studies of gene function, natural variation, and the evolution of recombination in Caenorhabditis nematodes.
Zdroje
1. MaupasE 1900 Modes et formes de reproduction des nematodes. Arch Zool Exp Gen 8 463 624
2. DoughertyECNigonV 1949 A new species of the free-living nematode genus Rhabditis of interest in comparative physiology and genetics. Journal of Parasitology 35 11
3. EdgarRSWoodWB 1977 The nematode C. elegans: A new organism for intensive biological study. Science 198 1285 1286
4. RiddleDLBlumenthalTMeyerBJPriessJR 1997 C. elegans II Cold Spring Harbor, NY Cold Spring Harbor Laboratory Press
5. NigonVDoughertyEC 1949 Reproductive patterns and attempts at reciprocal crossing of Rhabditis elegans Maupas, 1900, and Rhabditis briggsae Dougherty and Nigon, 1949 (Nematoda: rhabditidae). Journal of Experimental Zoology 112 485 503
6. FriedmanPAPlatzerEGEbyJE 1977 Species Differentiation in Caenorhabditis briggsae and Caenorhabditis elegans. Journal of Nematology 9 197 203
7. GuoYLangSEllisRE 2009 Independent Recruitment of F Box Genes to Regulate Hermaphrodite Development during Nematode Evolution. Current Biology 19 1853 1860
8. HillRCde CarvalhoCESalogiannisJSchlagerBPilgrimD 2006 Genetic flexibility in the convergent evolution of hermaphroditism in Caenorhabditis nematodes. Developmental Cell 10 531 538
9. KiontkeKFitchD The C. elegans Research Community, editor 2005 The phylogenetic relationships of Caenorhabditis and other rhabditids WormBook 1 11
10. KiontkeKGavinNPRaynesYRoehrigCPianoF 2004 Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss. Proceedings of the National Academy of Sciences, USA 101 9003 9008
11. NayakSGoreeJSchedlT 2005 fog-2 and the evolution of self-fertile hermaphroditism in Caenorhabditis. PLoS Biol 3 e6 doi:10.1371/journal.pbio.0030006
12. LinKTBroitman-MaduroGHungWWCervantesSMaduroMF 2009 Knockdown of SKN-1 and the Wnt effector TCF/POP-1 reveals differences in endomesoderm specification in C. briggsae as compared with C. elegans. Developmental Biology 325 296 306
13. WangXChamberlinH 2002 Multiple regulatory changes contribute to the evolution of the Caenorhabditis lin-48 ovo gene. Genes & Development 16 2345 2349
14. WangXChamberlinHM 2004 Evolutionary innovation of the excretory system in Caenorhabditis elegans. Nature Genetics 36 231 232
15. RockmanMVKruglyakL 2009 Recombinational landscape and population genomics of Caenorhabditis elegans. PLoS Genet 5 e1000419 doi:10.1371/journal.pgen.1000419
16. GrausteinAGasparJMWaltersJRPalopoliMF 2002 Levels of DNA polymorphism vary with mating system in the nematode genus Caenorhabditis. Genetics 161 99 107
17. DolginESFelixMACutterAD 2008 Hakuna Nematoda: genetic and phenotypic diversity in African isolates of Caenorhabditis elegans and C. briggsae. Heredity 100 304 315
18. CutterAD 2006 Nucleotide polymorphism and linkage disequilibrium in wild populations of the partial selfer Caenorhabditis elegans. Genetics 172 171 184
19. DenverDRMorrisKThomasWK 2003 Phylogenetics in Caenorhabditis elegans: an analysis of divergence and outcrossing. Molecular Biology and Evolution 20 393 400
20. HaberMSchungelMPutzAMullerSHasertB 2005 Evolutionary history of Caenorhabditis elegans inferred from microsatellites: evidence for spatial and temporal genetic differentiation and the occurrence of outbreeding. Molecular Biology and Evolution 22 160 173
21. SivasundarAHeyJ 2003 Population genetics of Caenorhabditis elegans: the paradox of low polymorphism in a widespread species. Genetics 163 147 157
22. SivasundarAHeyJ 2005 Sampling from natural populations with RNAi reveals high outcrossing and population structure in Caenorhabditis elegans. Current Biology 15 1598 1602
23. SwanKACurtisDEMcKusickKBVoinovAVMapaFA 2002 High-throughput gene mapping in Caenorhabditis elegans. Genome Research 12 1100 1105
24. BarriéreAFélixMA 2005 High local genetic diversity and low outcrossing rate in Caenorhabditis elegans natural populations. Current Biology 15 1176 1184
25. CutterADChoiJY 2010 Natural selection shapes nucleotide polymorphism across the genome of the nematode Caenorhabditis briggsae. Genome Research 20 1103 1111
26. CutterADYanWTsvetkovNSunilSFelixMA 2010 Molecular population genetics and phenotypic sensitivity to ethanol for a globally diverse sample of the nematode Caenorhabditis briggsae. Molecular Ecology 19 798 809
27. HoweDKDenverDR 2008 Muller's Ratchet and compensatory mutation in Caenorhabditis briggsae mitochondrial genome evolution. BMC Evolutionary Biology 8 62
28. CutterADFelixMABarriereACharlesworthD 2006 Patterns of nucleotide polymorphism distinguish temperate and tropical wild isolates of Caenorhabditis briggsae. Genetics 173 2021 2031
29. SeidelHSRockmanMVKruglyakL 2008 Widespread genetic incompatibility in C. elegans maintained by balancing selection. Science 319 589 594
30. BairdS 2001 Strain-specific variation in the pattern of caudal papillae in Caenorhabidits briggsae (Nematoda: Rhabditidae); implication for species identification. Nematology 3 373 376
31. BairdSEDavidsonCRBohrerJC 2005 The genetics of ray pattern variation in Caenorhabditis briggsae. BMC Evolutionary Biology 5 3
32. DelattreMFelixMA 2001 Development and evolution of a variable left-right asymmetry in nematodes: the handedness of P11/P12 migration. Developmental Biology 232 362 371
33. FodorARiddleDLNelsonFKGoldenJW 1983 Comparison of a new wild-type Caenorhabditis briggsae with laboratory strains of C. briggsae and C. elegans. Nematologica 29 203 217
34. HodgkinJDoniachT 1997 Natural variation and copulatory plug formation in Caenorhabditis elegans. Genetics 146 149 164
35. PalopoliMFRockmanMVTinMaungARamsayCCurwenS 2008 Molecular basis of the copulatory plug polymorphism in Caenorhabditis elegans. Nature 454 1019 1022
36. WangXGreenbergJFChamberlinHM 2004 Evolution of regulatory elements producing a conserved gene expression pattern in Caenorhabditis. Evolution and Development 6 237 245
37. SteinLDBaoZBlasiarDBlumenthalTBrentMR 2003 The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics. PLoS Biol 1 e45 doi:10.1371/journal.pbio.0000045
38. HillierLWMillerRDBairdSEChinwallaAFultonLA 2007 Comparison of C. elegans and C. briggsae Genome Sequences Reveals Extensive Conservation of Chromosome Organization and Synteny. PLoS Biol 5 e167 doi:10.1371/journal.pbio.0050167
39. KoboldtDCStaischJThillainathanBHainesKBairdSE 2010 A toolkit for rapid gene mapping in the nematode Caenorhabditis briggsae. BMC Genomics 11 236
40. ZhaoZFlibotteSMurrayJIBlickDBoyleTJ 2010 New tools for investigating the comparative biology of Caenorhabditis briggsae and C. elegans. Genetics 184 853 863
41. BalasubramanianSSchwartzCSinghAWarthmannNKimMC 2009 QTL mapping in new Arabidopsis thaliana advanced intercross-recombinant inbred lines. PLoS ONE 4 e4318 doi:10.1371/journal.pone.0004318
42. Balint-KurtiPJZwonitzerJCWisserRJCarsonMLOropeza-RosasMA 2007 Precise mapping of quantitative trait loci for resistance to southern leaf blight, caused by Cochliobolus heterostrophus race O, and flowering time using advanced intercross maize lines. Genetics 176 645 657
43. SchwartzCBalasubramanianSWarthmannNMichaelTPLempeJ 2009 Cis-regulatory changes at FLOWERING LOCUS T mediate natural variation in flowering responses of Arabidopsis thaliana. Genetics 183 723 732, 721SI–727SI
44. DarvasiASollerM 1995 Advanced intercross lines, an experimental population for fine genetic mapping. Genetics 141 1199 1207
45. HammarlundMDavisMWNguyenHDaytonDJorgensenEM 2005 Heterozygous insertions alter crossover distribution but allow crossover interference in Caenorhabditis elegans. Genetics 171 1047 1056
46. DobzhanskyTEplingC 1948 The suppression of crossing over in inversion heterozygotes of Drosophila pseudoobscura. Proceedings of the National Academy of Sciences, USA 34 137 141
47. RobbinsLG 1974 Exchange within heterozygous inversions in Drosophila melanogaster. Genetics 77 105 114
48. NurU 1968 Synapsis and crossing over within a paracentric inversion in the grasshopper, Camnula pellucida. Chromosoma 25 198 214
49. StumpADPombiMGoeddelLRibeiroJMWilderJA 2007 Genetic exchange in 2La inversion heterokaryotypes of Anopheles gambiae. Insect Molecular Biology 16 703 709
50. PeguerolesCOrdonezVMestresFPascualM 2010 Recombination and selection in the maintenance of the adaptive value of inversions. Journal of Evolutionary Biology 23 2709 2717
51. KoehlerKEMillieEACherryJPSchrumpSEHassoldTJ 2004 Meiotic exchange and segregation in female mice heterozygous for paracentric inversions. Genetics 166 1199 1214
52. WhiteMJD 1978 Modes of speciation San Fransisco W. H. Freeman
53. LandeR 1979 Effective deme sizes during long-term evolution estimated from rates of chromosomal rearrangement. Evolution 33 234 251
54. KirkpatrickMBartonN 2006 Chromosome inversions, local adaptation and speciation. Genetics 173 419 434
55. LowryDBWillisJH 2010 A widespread chromosomal inversion polymorphism contributes to a major life-history transition, local adaptation, and reproductive isolation. PLoS Biol 8 e1000500 doi:10.1371/journal.pbio.1000500
56. KirkpatrickM 2010 How and Why Chromosome Inversions Evolve. PLoS Biol 8 e1000501 doi:10.1371/journal.pbio.1000501
57. MeneelyPFaragoAKauffmanT 2002 Crossover distribution and high interference for both the X chromosome and an autosome during oogenesis and spermatogenesis in Caenorhabditis elegans. Genetics 162 1169 1177
58. KelleherDFde CarvalhoCEDotyAVLaytonMChengAT 2008 Comparative genetics of sex determination: masculinizing mutations in Caenorhabditis briggsae. Genetics 178 1415 1429
59. ChakravartiA 1991 A graphical representation of genetic and physical maps: The Marey map. Genomics 11 219 222
60. AlbertsonDThomsonJ 1982 The kinetochores of Caenorhabditis elegans. Chromosoma 86 409 428
61. LewontinRC 1964 The interaction of selection and linkage. I. General considerations; heterotic models. Genetics 49 49 67
62. YamamotoKNohataJKadono-OkudaKNarukawaJSasanumaM 2008 A BAC-based integrated linkage map of the silkworm Bombyx mori. Genome Biology 9 R21
63. SolignacMMougelFVautrinDMonnerotMCornuetJM 2007 A third-generation microsatellite-based linkage map of the honey bee, Apis mellifera, and its comparison with the sequence-based physical map. Genome Biology 8 R66
64. LiXRamchiaryNChoiSRVan NguyenDHossainMJ 2010 Development of a high density integrated reference genetic linkage map for the multinational Brassica rapa Genome Sequencing Project. Genome 53 939 947
65. NiehuisOGibsonJDRosenbergMSPannebakkerBAKoevoetsT 2010 Recombination and its impact on the genome of the haplodiploid parasitoid wasp Nasonia. PLoS ONE 5 e8597 doi:10.1371/journal.pone.0008597
66. WerrenJHRichardsSDesjardinsCANiehuisOGadauJ 2010 Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327 343 348
67. TweedieSAshburnerMFallsKLeylandPMcQuiltonP 2009 FlyBase: enhancing Drosophila Gene Ontology annotations. Nucleic Acids Research 37 D555 559
68. BurkeJMLaiZSalmasoMNakazatoTTangS 2004 Comparative mapping and rapid karyotypic evolution in the genus Helianthus. Genetics 167 449 457
69. TrueJRMercerJMLaurieCC 1996 Differences in crossover frequency and distribution among three sibling species of Drosophila. Genetics 142 507 523
70. StevisonLSNoorMA 2010 Genetic and evolutionary correlates of fine-scale recombination rate variation in Drosophila persimilis. Journal of Molecular Evolution 71 332 345
71. CutterAD 2008 Divergence times in Caenorhabditis and Drosophila inferred from direct estimates of the neutral mutation rate. Molecular Biology and Evolution 25 778 786
72. DumontBLWhiteMASteffyBWiltshireTPayseurBA 2011 Extensive recombination rate variation in the house mouse species complex inferred from genetic linkage maps. Genome Research 21 114 125
73. BeukeboomLWNiehuisOPannebakkerBAKoevoetsTGibsonJD 2010 A comparison of recombination frequencies in intraspecific versus interspecific mapping populations of Nasonia. Heredity 104 302 309
74. MetsDGMeyerBJ 2009 Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure. Cell 139 73 86
75. TsaiCJMetsDGAlbrechtMRNixPChanA 2008 Meiotic crossover number and distribution are regulated by a dosage compensation protein that resembles a condensin subunit. Genes & Development 22 194 211
76. WagnerCRKuerversLBaillieDLYanowitzJL 2010 xnd-1 regulates the global recombination landscape in Caenorhabditis elegans. Nature 467 839 843
77. LiuTRechtsteinerAEgelhoferTAVielleALatorreI 2011 Broad chromosomal domains of histone modification patterns in C. elegans. Genome Research 21 227 236
78. MacQueenAJPhillipsCMBhallaNWeiserPVilleneuveAM 2005 Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell 123 1037 1050
79. DobzhanskyT 1936 Studies on hybrid sterility. II. Localization of sterility factors in Drosophila pseudoobscura hybrids. Genetics 21 113 135
80. MullerHJ 1939 Reversibility in evolution considered from the standpoint of genetics. Biological Reviews of the Cambridge Philosophical Society 14 261 280
81. MullerHJ 1940 Bearing of the Drosophila work on systematics. HuxleyJ The New Systematics Oxford Clarendon Press 185 268
82. WangJChenPJWangGJKellerL 2010 Chromosome size differences may affect meiosis and genome size. Science 329 293
83. MaydanJSLorchAEdgleyMLFlibotteSMoermanDG 2010 Copy number variation in the genomes of twelve natural isolates of Caenorhabditis elegans. BMC Genomics 11 62
84. HurstGDWerrenJH 2001 The role of selfish genetic elements in eukaryotic evolution. Nature Reviews: Genetics 2 597 606
85. LyttleTW 1991 Segregation distorters. Annual Review of Genetics 25 511 557
86. TaylorDRIngvarssonPK 2003 Common features of segregation distortion in plants and animals. Genetica 117 27 35
87. DobzhanskyT 1937 Genetics and the Origin of Species New York Columbia University Press
88. CoyneJAOrrHA 2004 Speciation Sunderland, Massachusetts Sinauer
89. PoytonROMcEwenJE 1996 Crosstalk between nuclear and mitochondrial genomes. Annual Review of Biochemistry 65 563 607
90. BlierPUDufresneFBurtonRS 2001 Natural selection and the evolution of mtDNA-encoded peptides: evidence for intergenomic co-adaptation. Trends in Genetics 17 400 406
91. GershoniMTempletonARMishmarD 2009 Mitochondrial bioenergetics as a major motive force of speciation. Bioessays 31 642 650
92. BombliesKWeigelD 2010 Arabidopsis and relatives as models for the study of genetic and genomic incompatibilities. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 365 1815 1823
93. RiesebergLHArcherMAWayneRK 1999 Transgressive segregation, adaptation and speciation. Heredity 83 363 372
94. HallMCWillisJH 2005 Transmission ratio distortion in intraspecific hybrids of Mimulus guttatus: implications for genomic divergence. Genetics 170 375 386
95. FishmanLKellyAJMorganEWillisJH 2001 A genetic map in the Mimulus guttatus species complex reveals transmission ratio distortion due to heterospecific interactions. Genetics 159 1701 1716
96. NiehuisOJudsonAKGadauJ 2008 Cytonuclear genic incompatibilities cause increased mortality in male F2 hybrids of Nasonia giraulti and N. vitripennis. Genetics 178 413 426
97. McDanielSFWillisJHShawAJ 2007 A linkage map reveals a complex basis for segregation distortion in an interpopulation cross in the moss Ceratodon purpureus. Genetics 176 2489 2500
98. MoyleLCGrahamEB 2006 Proceedings of the SMBE Tri-National Young Investigators' Workshop 2005. Genome-wide associations between hybrid sterility QTL and marker transmission ratio distortion. Molecular Biology and Evolution 23 973 980
99. RandDMHaneyRAFryAJ 2004 Cytonuclear coevolution: the genomics of cooperation. Trends in Ecology & Evolution 19 645 653
100. ChevironZABrumfieldRT 2009 Migration-selection balance and local adaptation of mitochondrial haplotypes in rufous-collared sparrows (Zonotrichia capensis) along an elevational gradient. Evolution 63 1593 1605
101. EllisonCKBurtonRS 2008 Interpopulation hybrid breakdown maps to the mitochondrial genome. Evolution 62 631 638
102. HoweDKBaerCFDenverDR 2010 High rate of large deletions in Caenorhabditis briggsae mitochondrial genome mutation processes. Genome Biology and Evolution 2 29 38
103. BallardJWMelvinRGKatewaSDMaasK 2007 Mitochondrial DNA variation is associated with measurable differences in life-history traits and mitochondrial metabolism in Drosophila simulans. Evolution 61 1735 1747
104. EllisonCKNiehuisOGadauJ 2008 Hybrid breakdown and mitochondrial dysfunction in hybrids of Nasonia parasitoid wasps. Journal of Evolutionary Biology 21 1844 1851
105. SacktonTBHaneyRARandDM 2003 Cytonuclear coadaptation in Drosophila: disruption of cytochrome c oxidase activity in backcross genotypes. Evolution 57 2315 2325
106. ZeylCAndresonBWeninckE 2005 Nuclear-mitochondrial epistasis for fitness in Saccharomyces cerevisiae. Evolution 59 910 914
107. KaoKCSchwartzKSherlockG 2010 A genome-wide analysis reveals no nuclear Dobzhansky-Muller pairs of determinants of speciation between S. cerevisiae and S. paradoxus, but suggests more complex incompatibilities. PLoS Genet 6 e1001038 doi:10.1371/journal.pgen.1001038
108. JohnsonNA 2010 Hybrid incompatibility genes: remnants of a genomic battlefield? Trends in Genetics 26 317 325
109. PresgravesDC 2010 The molecular evolutionary basis of species formation. Nature Reviews: Genetics 11 175 180
110. PrasadACroydon-SugarmanMJMurrayRLCutterAD 2011 Temperature-Dependent Fecundity Associates with Latitude in Caenorhabditis briggsae. Evolution 65 52 63
111. Joyner-MatosJUpadhyayASalomonMPGrigaltchikVBaerCF 2009 Genetic (Co)variation for life span in rhabditid nematodes: role of mutation, selection, and history. J Gerontol A Biol Sci Med Sci 64 1134 1145
112. EstesSColeman-HulbertALHicksKAde HaanGMarthaSR 2011 Natural variation in life history and aging phenotypes is associated with mitochondrial DNA deletion frequency in Caenorhabditis briggsae. BMC Evolutionary Biology 11 11
113. DolginESCharlesworthBBairdSECutterAD 2007 Inbreeding and outbreeding depression in Caenorhabditis nematodes. Evolution 61 1339 1352
114. RockmanMVSkrovanekSSKruglyakL 2010 Selection at linked sites shapes heritable phenotypic variation in C. elegans. Science 330 372 376
115. HillKLL'HernaultSW 2001 Analyses of reproductive interactions that occur after heterospecific matings within the genus Caenorhabditis. Developmental Biology 232 105 114
116. BairdS 2002 Haldane's Rule by sexual transformation in Caenorhabditis. Genetics 161 1349 1353
117. BairdSESutherlinMEEmmonsSW 1992 Reproductive isolation in Rhabditidae (Nematoda: Secernentea): mechanisms that isolate six species of three genera. Evolution 46 585 594
118. BairdSEYenWC 2000 Reproductive isolation in Caenorhabditis: terminal phenotypes of hybrid embryos. Evolution and Development 2 9 15
119. WoodruffGCEkeOBairdSEFelixMAHaagES 2010 Insights into species divergence and the evolution of hermaphroditism from fertile interspecies hybrids of Caenorhabditis nematodes. Genetics 186 997 1012
120. FanJBOliphantAShenRKermaniBGGarciaF 2003 Highly parallel SNP genotyping. Cold Spring Harb Symp Quant Biol 68 69 78
121. ManlyKFCudmoreRHJrMeerJM 2001 Map Manager QTX, cross-platform software for genetic mapping. Mammalian Genome 12 930 932
122. MuggeoVM 2003 Estimating regression models with unknown break-points. Statistics in Medicine 22 3055 3071
123. JurkaJ 2000 Repbase update: a database and an electronic journal of repetitive elements. Trends in Genetics 16 418 420
124. DelcherALPhillippyACarltonJSalzbergSL 2002 Fast algorithms for large-scale genome alignment and comparison. Nucleic Acids Research 30 2478 2483
125. DawdyDRMatalasNC 1964 Satistical and probability analysis of hydrologic data, part III: analysis of variance, covariance, and time series. ChowVT Handbook of applied hydrology, a compendium of water-resources technology New York McGraw-Hill 68 90
126. HahnMW 2006 Proceedings of the SMBE Tri-National Young Investigators' Workshop 2005. Accurate inference and estimation in population genomics. Molecular Biology and Evolution 23 911 918
127. WhiteBJHahnMWPombiMCassoneBJLoboNF 2007 Localization of candidate regions maintaining a common polymorphic inversion (2La) in Anopheles gambiae. PLoS Genet 3 e217 doi:10.1371/journal.pgen.0030217
128. BarrettJCFryBMallerJDalyMJ 2005 Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21 263 265
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Genetika Reprodukčná medicínaČlánok vyšiel v časopise
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