The Genetic Architecture of Natural Variation in Recombination Rate in Drosophila melanogaster

PLoS Genetics

Volumn 12, Issue 4, 2016, Pages

  Hunter, Chad M ^a   Huang, Wen ^a   Mackay, Trudy F C ^a   Singh, Nadia D ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; FUNCTIONAL ASSESSMENT; GENETIC RECOMBINATION; GENETIC VARIATION; GENOME-WIDE ASSOCIATION STUDY; HEREDITY; MEIOTIC RECOMBINATION; NONHUMAN; QUANTITATIVE TRAIT; WOLBACHIA; X CHROMOSOME; ANIMAL; FEMALE; GENETICS; ISOLATION AND PURIFICATION; MALE; MICROBIOLOGY;

ANIMALS; DROSOPHILA MELANOGASTER; FEMALE; GENOME-WIDE ASSOCIATION STUDY; MALE; RECOMBINATION, GENETIC; WOLBACHIA;

EID: 84964832412     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005951     Document Type: Article

References (183)

1. Roeder GS, Meiotic chromosomes: it takes two to tango. Genes Dev. 1997;11: 2600–2621. 9334324
2. Lindsley DL, Sandler L, Counce SJ, Chandley AC, Lewis KR, The genetic analysis of meiosis in female Drosophila melanogaster. Philos Trans R Soc Lond. 1977;277: 295–312.
3. Kong A, Gudbjartsson DF, Sainz J, Jonsdottir GM, Gudjonsson SA, Richardsson B, et al. A high-resolution recombination map of the human genome. Nat Genet. 2002;31: 241–247. 12053178
4. Crawford DC, Bhangale T, Li N, Hellenthal G, Rieder MJ, Nickerson DA, et al. Evidence for substantial fine-scale variation in recombination rates across the human genome. Nat Genet. 2004;36: 700–706. doi: 10.1038/ng137615184900
5. McVean GAT, Myers SR, Hunt S, Deloukas P, Bentley DR, Donnelly P, The fine-scale structure of recombination rate variation in the human genome. Science. 2004;304: 581–584. 15105499
6. Myers S, Bottolo L, Freeman C, McVean G, Donnelly P, A fine-scale map of recombination rates and hotspots across the human genome. Science. 2005;310: 321–324. 16224025
7. Cirulli ET, Kliman RM, Noor MAF, Fine-scale crossover rate heterogeneity in Drosophila pseudoobscura. J Mol Evol. 2007;64: 129–135. 17160365
8. Mancera E, Bourgon R, Brozzi A, Huber W, Steinmetz LM, High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature. 2008;454: 479–483. doi: 10.1038/nature0713518615017
9. Paigen K, Szatkiewicz JP, Sawyer K, Leahy N, Parvanov ED, Ng SHS, et al. The recombinational anatomy of a mouse chromosome. PLoS Genet. 2008;4: e1000119. doi: 10.1371/journal.pgen.100011918617997
10. Singh ND, Aquadro CF, Clark AG, Estimation of fine-scale recombination intensity variation in the white-echinus interval of D. melanogaster. J Mol Evol. 2009;69: 42–53. doi: 10.1007/s00239-009-9250-519504037
11. Singh ND, Stone EA, Aquadro CF, Clark AG, Fine-scale heterogeneity in crossover rate in the garnet-scalloped region of the Drosophila melanogaster X chromosome. Genetics. 2013;194: 375–387. doi: 10.1534/genetics.112.14674623410829
12. Comeron JM, Ratnappan R, Bailin S, The many landscapes of recombination in Drosophila melanogaster. PLoS Genet. 2012;8: e1002905. doi: 10.1371/journal.pgen.100290523071443
13. Brooks LD, Marks RW, The organization of genetic variation for recombination in Drosophila melanogaster. Genetics. 1986;114: 525–547. 3095185
14. Rahn MI, Solari AJ, Recombination nodules in the oocytes of the chicken, Gallus domesticus. Cytogenet Cell Genet. 1986;43: 187–193. 3802921
15. Barnes TM, Kohara Y, Coulson A, Hekimi S, Meiotic recombination, noncoding DNA and genomic organization in Caenorhabditis elegans. Genetics. 1995;141: 159–179. 8536965
16. True JR, Mercer JM, Laurie CC, Differences in crossover frequency and distribution among three sibling species of Drosophila. Genetics. 1996;142: 507–523. 8852849
17. Wall JD, Frisse LA, Hudson RR, Rienzo AD, Comparative linkage-disequilibrium analysis of the b-globin hotspot in primates. Am J Hum Genet. 2003;73: 1330–1340. 14628290
18. Ptak SE, Roeder AD, Stephens M, Gilad Y, Paabo S, Przeworski M, Absence of the TAP2 human recombination hotspot in chimpanzees. PLoS Biol. 2004;2: 849–855.
19. Ptak SE, Hinds DA, Koehler K, Nickel B, Patil N, Ballinger DG, et al. Fine-scale recombination patterns differ between chimpanzees and humans. Nat Genet. 2005;37: 429–434. 15723063
20. Fearnhead P, Smith NGC, A novel method with improved power to detect recombination hotspots from polymorphism data reveals multiple hotspots in human genes. Am J Hum Genet. 2005;77: 781–794. 16252238
21. Winckler W, Myers SR, Richter DJ, Onofrio RC, McDonald GJ, Bontrop RE, et al. Comparison of fine-scale recombination rates in humans and chimpanzees. Science. 2005;308: 107–111. 15705809
22. Wilfert L, Gadau J, Schmid-Hempel P, Variation in genomic recombination rates among animal taxa and the case of social insects. Heredity. 2007;98: 189–197. doi: 10.1038/sj.hdy.680095017389895
23. Dumont BL, Broman KW, Payseur BA, Variation in genomic recombination rates among heterogeneous stock mice. Genetics. 2009;182: 1345–1349. doi: 10.1534/genetics.109.10511419535547
24. Rockman MV, Kruglyak L, Recombinational landscape and population genomics of Caenorhabditis elegans. PLoS Genet. 2009;5: e1000419. doi: 10.1371/journal.pgen.100041919283065
25. Bauer E, Falque M, Walter H, Bauland C, Camisan C, Campo L, et al. Intraspecific variation of recombination rate in maize. Genome Biol. 2013;14: R103. 24050704
26. Ross C, DeFelice D, Hunt G, Ihle K, Rueppell O, Rychtář J, Chhetri M, Gupta S, Shivaji R, A comparison of multiple genome-wide recombination maps in Apis mellifera. In: Collaborative mathematics and statistics research. Springer International Publishing; 2015. pp. 91–98. Available: http://link.springer.com/chapter/10.1007/978-3-319-11125-4_10
27. Fisher RA, The genetical theory of natural selection. Oxford, England: Clarendon Press; 1930.
28. Muller HJ, Some genetic aspects of sex. Am Nat. 1932;66: 118–138.
29. Hill WG, Robertson A, The effect of linkage on limits to artificial selection. Genet Res. 1966;8: 269–294. 5980116
30. Aguadé M, Miyashita N, Langley CH, Reduced variation in the yellow-achaete-scute region in natural populations of Drosophila melanogaster. Genetics. 1989;122: 607–615. 17246506
31. Stephan W, Langley CH, Molecular genetic variation in the centromeric region of the X chromosome in three Drosophila ananassae populations. I. Contrasts between the vermilion and forked loci. Genetics. 1989;121: 89–99. 2563714
32. Begun DJ, Aquadro CF, Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature. 1992;356: 519–520. 1560824
33. Pál C, Papp B, Hurst LD, Does the recombination rate affect the efficiency of purifying selection? The yeast genome provides a partial answer. Mol Biol Evol. 2001;18: 2323–2326. 11719582
34. Betancourt AJ, Presgraves DC, Linkage limits the power of natural selection in Drosophila. PNAS. 2002;99: 13616–13620. 12370444
35. Bartolome C, Maside X, Charlesworth B, On the abundance and distribution of transposable elements in the genome of Drosophila melanogaster. Mol Biol Evol. 2002;19: 926–937. 12032249
36. Rizzon C, Marais G, Gouy M, Biemont C, Recombination rate and the distribution of transposable elements in the Drosophila melanogaster genome. Genome Res. 2002;12: 400–407. 11875027
37. Petrov DA, Fiston-Lavier A-S, Lipatov M, Lenkov K, González J, Population genomics of transposable elements in Drosophila melanogaster. Mol Biol Evol. 2011;28: 1633–1644. doi: 10.1093/molbev/msq33721172826
38. Kofler R, Betancourt AJ, Schlötterer C, Sequencing of pooled DNA samples (Pool-Seq) uncovers complex dynamics of transposable element insertions in Drosophila melanogaster. PLoS Genet. 2012;8: e1002487. doi: 10.1371/journal.pgen.100248722291611
39. Stephan W, Recombination and the evolution of satellite DNA. Genet Res. 1986;47: 167–174. doi: 10.1017/S00166723000230893744043
40. Stephan W, Quantitative variation and chromosomal location of satellite DNAs. Genet Res. 1987;50: 41–52. doi: 10.1017/S00166723000233263653688
41. Comeron JM, Kreitman M, Aguadé M, Natural selection on synonymous sites is correlated with gene length and recombination in Drosophila. Genetics. 1999;151: 239–249. 9872963
42. Marais G, Piganeau G, Hill-Robertson interference is a minor determinant of variations in codon bias across Drosophila melanogaster and Caenorhabditis elegans genomes. Mol Biol Evol. 2002;19: 1399–1406. 12200468
43. Baudat F, Buard J, Grey C, Fledel-Alon A, Ober C, Przeworski M, et al. PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science. 2010;327: 836–840. doi: 10.1126/science.118343920044539
44. Myers S, Bowden R, Tumian A, Bontrop RE, Freeman C, MacFie TS, et al. Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science. 2010;327: 876–879. doi: 10.1126/science.118236320044541
45. Parvanov ED, Petkov PM, Paigen K, Prdm9 controls activation of mammalian recombination hotspots. Science. 2010;327: 835. doi: 10.1126/science.118149520044538
46. Berg IL, Neumann R, Lam K-WG, Sarbajna S, Odenthal-Hesse L, May CA, et al. PRDM9 variation strongly influences recombination hot-spot activity and meiotic instability in humans. Nat Genet. 2010;42: 859–863. doi: 10.1038/ng.65820818382
47. Baudat F, Imai Y, de Massy B, Meiotic recombination in mammals: localization and regulation. Nat Rev Genet. 2013;14: 794–806. doi: 10.1038/nrg357324136506
48. Oliver PL, Goodstadt L, Bayes JJ, Birtle Z, Roach KC, Phadnis N, et al. Accelerated evolution of the Prdm9 speciation gene across diverse metazoan taxa. PLoS Genet. 2009;5: 1–14.
49. Mihola O, Trachtulec Z, Vlcek C, Schimenti JC, Forejt J, A mouse speciation gene encodes a meiotic histone H3 methyltransferase. Science. 2009;323: 373–375. doi: 10.1126/science.116360119074312
50. Berg IL, Neumann R, Sarbajna S, Odenthal-Hesse L, Butler NJ, Jeffreys AJ, Variants of the protein PRDM9 differentially regulate a set of human meiotic recombination hotspots highly active in African populations. Proc Natl Acad Sci U S A. 2011;108: 12378–12383. doi: 10.1073/pnas.110953110821750151
51. Kong A, Thorleifsson G, Gudbjartsson DF, Masson G, Sigurdsson A, Jonasdottir A, et al. Fine-scale recombination rate differences between sexes, populations and individuals. Nature. 2010;467: 1099–1103. doi: 10.1038/nature0952520981099
52. Hinch AG, Tandon A, Patterson N, Song Y, Rohland N, Palmer CD, et al. The landscape of recombination in African Americans. Nature. 2011;476: 170–175. doi: 10.1038/nature1033621775986
53. Smagulova F, Gregoretti IV, Brick K, Khil P, Camerini-Otero RD, Petukhova GV, Genome-wide analysis reveals novel molecular features of mouse recombination hotspots. Nature. 2011;472: 375–378. doi: 10.1038/nature0986921460839
54. Auton A, Fledel-Alon A, Pfeifer S, Venn O, Ségurel L, Street T, et al. A fine-scale chimpanzee genetic map from population sequencing. Science. 2012;336: 193–198. doi: 10.1126/science.121687222422862
55. Brick K, Smagulova F, Khil P, Camerini-Otero RD, Petukhova GV, Genetic recombination is directed away from functional genomic elements in mice. Nature. 2012;485: 642–645. doi: 10.1038/nature1108922660327
56. Kulathinal RJ, Bennett SM, Fitzpatrick CL, Noor MAF, Fine-scale mapping of recombination rate in Drosophila refines its correlation to diversity and divergence. PNAS. 2008;105: 10051–10056. doi: 10.1073/pnas.080184810518621713
57. Stevison LS, Noor MAF, Genetic and evolutionary correlates of fine-scale recombination rate variation in Drosophila persimilis. J Mol Evol. 2010;71: 332–345. doi: 10.1007/s00239-010-9388-120890595
58. Heil CSS, Noor MAF, Zinc finger binding motifs do not explain recombination rate variation within or between species of Drosophila. PLoS ONE. 2012;7: e45055. doi: 10.1371/journal.pone.004505523028758
59. Miller DE, Takeo S, Nandanan K, Paulson A, Gogol MM, Noll AC, et al. A whole-chromosome analysis of meiotic recombination in Drosophila melanogaster. Genes Genomes Genet. 2012;2: 249–260.
60. Kaur T, Rockman MV, Crossover heterogeneity in the absence of hotspots in Caenorhabditis elegans. Genetics. 2014;196: 137–148. doi: 10.1534/genetics.113.15885724172135
61. Kong A, Thorleifsson G, Stefansson H, Masson G, Helgason A, Gudbjartsson DF, et al. Sequence variants in the RNF212 gene associate with genome-wide recombination rate. Science. 2008;319: 1398–1401. doi: 10.1126/science.115242218239089
62. Chowdhury R, Bois PRJ, Feingold E, Sherman SL, Cheung VG, Genetic analysis of variation in human meiotic recombination. PLoS Genet. 2009;5: e1000648. doi: 10.1371/journal.pgen.100064819763160
63. Sandor C, Li W, Coppieters W, Druet T, Charlier C, Georges M, Genetic variants in REC8, RNF212, and PRDM9 influence male recombination in cattle. PLoS Genet. 2012;8: e1002854. doi: 10.1371/journal.pgen.100285422844258
64. Johnston SE, Slate J, Pemberton JM, A genomic region containing RNF212 is associated with sexually-dimorphic recombination rate variation in wild Soay sheep (Ovis aries). bioRxiv. 2015; 024869. doi: 10.1101/024869
65. Reynolds A, Qiao H, Yang Y, Chen JK, Jackson N, Biswas K, et al. RNF212 is a dosage-sensitive regulator of crossing-over during mammalian meiosis. Nat Genet. 2013;45: 269–278. doi: 10.1038/ng.254123396135
66. Capilla L, Medarde N, Alemany-Schmidt A, Oliver-Bonet M, Ventura J, Ruiz-Herrera A, Genetic recombination variation in wild Robertsonian mice: on the role of chromosomal fusions and Prdm9 allelic background. Proc R Soc Lond B Biol Sci. 2014;281: 20140297. doi: 10.1098/rspb.2014.0297
67. Bhatt AM, Lister C, Page T, Fransz P, Findlay K, Jones GH, et al. The DIF1 gene of Arabidopsis is required for meiotic chromosome segregation and belongs to the REC8/RAD21 cohesin gene family. Plant J. 1999;19: 463–472. doi: 10.1046/j.1365-313X.1999.00548.x10504568
68. Parisi S, McKay MJ, Molnar M, Thompson MA, van der Spek PJ, van Drunen-Schoenmaker E, et al. Rec8p, a meiotic recombination and sister chromatid cohesion phosphoprotein of the Rad21p family conserved from fission yeast to humans. Mol Cell Biol. 1999;19: 3515–3528. 10207075
69. Watanabe Y, Nurse P, Cohesin Rec8 is required for reductional chromosome segregation at meiosis. Nature. 1999;400: 461–464. 10440376
70. Stefansson H, Helgason A, Thorleifsson G, Steinthorsdottir V, Masson G, Barnard J, et al. A common inversion under selection in Europeans. Nat Genet. 2005;37: 129–137. 15654335
71. Broadhead RS, Kidwell JF, Kidwell MG, Variation of the recombination fraction in Drosophila melanogaster females. J Hered. 1977;68: 323–326. 413856
72. Hunter CM, Singh ND, Do males matter? Testing the effects of male genetic background on female meiotic crossover rates in Drosophila melanogaster. Evolution. 2014;68: 2718–2726. doi: 10.1111/evo.1245524889512
73. Detlefsen JA, Roberts E, Studies on crossing over—I. The effect of selection on crossover values. J Exp Zool. 1921;32: 333–354.
74. Parsons PA, Selection for increased recombination in Drosophila melanogaster. Am Nat. 1958;92: 255–256.
75. Mukherjee AS, Effect of selection on crossing over in the males of Drosophila ananassae. Am Nat. 1961;95: 57–59.
76. Moyer SE, Selection for modification of recombination frequency of linked genes. University of Minnesota. 1964.
77. Chinnici JP, Modification of recombination frequency in Drosophila. II. The polygenic control of crossing over. Genetics. 1971;69: 85–96. 5002415
78. Chinnici JP, Modification of recombination frequency in Drosophila. I. Selection for increased and decreased crossing over. Genetics. 1971;69: 71–83. 5002414
79. Kidwell MG, Genetic change of recombination value in Drosophila melanogaster. I. Artificial selection for high and low recombination and some properties of recombination-modifying genes. Genetics. 1972;70: 419–423. 4623519
80. Kidwell MG, Genetic change of recombination value in Drosophila melanogaster. II. Simulated natural selection. Genetics. 1972;70: 433–443. 4623520
81. Valentin J, Characterization of a meiotic control gene affecting recombination in Drosophila melanogaster. Hereditas. 1973;75: 5–22. doi: 10.1111/j.1601-5223.1973.tb01137.x4204896
82. Valentin J, Selection for altered recombination frequency in Drosophila melanogaster. Hereditas. 1973;74: 295–297. doi: 10.1111/j.1601-5223.1973.tb01132.x4202017
83. Charlesworth B, Charlesworth D, Genetic variation in recombination in Drosophila. II. Genetic analysis of a high recombination stock. Heredity. 1985;54: 85–98.
84. Charlesworth B, Charlesworth D, Genetic variation in recombination in Drosophila. I. Responses to selection and preliminary genetic analysis. Heredity. 1985;54: 71–83.
85. Charlesworth B, Mori I, Charlesworth D, Genetic variation in recombination in Drosophila. III. Regional effects on crossing over and effects on non-disjunction. Heredity. 1985;55: 209–221.
86. Rodell CF, Schipper MR, Keenan DK, Modes of selection and recombination response in Drosophila melanogaster. J Hered. 2004;95: 70–75. 14757732
87. Flexon PB, Rodell CF, Genetic recombination and directional selection for DDT resistance in Drosophila melanogaster. Nature. 1982;298: 672–674. doi: 10.1038/298672a06808396
88. Korol AB, Iliadit KG, Increased recombination frequencies resulting from directional selection for geotaxis in Drosophila. Heredity. 1994;72: 64–68. 8119830
89. Zhuchenko AA, Korol AB, Kovtyukh LP, Change of the crossing-over frequency in Drosophila during selection for resistance to temperature fluctuations. Genetics. 1985;67: 73–78.
90. Mackay TFC, Richards S, Stone EA, Barbadilla A, Ayroles JF, Zhu D, et al. The Drosophila melanogaster Genetic Reference Panel. Nature. 2012;482: 173–178. doi: 10.1038/nature1081122318601
91. Huang W, Massouras A, Inoue Y, Peiffer J, Rámia M, Tarone A, et al. Natural variation in genome architecture among 205 Drosophila melanogaster Genetic Reference Panel lines. Genome Res. 2014;24: 1193–1208. doi: 10.1101/gr.171546.11324714809
92. Dunn OJ, Estimation of the medians for dependent variables. Ann Math Stat. 1959;30: 192–197.
93. Dunn OJ, Multiple comparisons among means. J Am Stat Assoc. 1961;56: 52–64. doi: 10.1080/01621459.1961.10482090
94. Morgan TH, Bridges CB, Sex-linked inheritance in Drosophila. Washington, D.C.: Carnegie Institution of Washington; 1916.
95. Bridges CB, Morgan TH, The third-chromosome group of mutant characters of Drosophila melanogaster. Washington, D.C.: Carnegie Institution of Washington; 1923.
96. Schultz J, Redfield H, Interchromosomal effects on crossing over in Drosophila. Cold Spring Harb Symp Quant Biol. 1951;16: 175–197. 14942738
97. Lucchesi JT, Suzuki DT, The Interchromosomal control of recombination. Annu Rev Genet. 1968;2: 53–86.
98. dos Santos G, Schroeder AJ, Goodman JL, Strelets VB, Crosby MA, Thurmond J, et al. FlyBase: introduction of the Drosophila melanogaster release 6 reference genome assembly and large-scale migration of genome annotations. Nucleic Acids Res. 2015;43: D690–D697. doi: 10.1093/nar/gku109925398896
99. Chintapalli VR, Wang J, Dow JAT, Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat Genet. 2007;39: 715–720. doi: 10.1038/ng204917534367
100. Celniker SE, Dillon LAL, Gerstein MB, Gunsalus KC, Henikoff S, Karpen GH, et al. Unlocking the secrets of the genome. Nature. 2009;459: 927–930. doi: 10.1038/459927a19536255
101. Adrian AB, Comeron JM, The Drosophila early ovarian transcriptome provides insight to the molecular causes of recombination rate variation across genomes. BMC Genomics. 2013;14: 794. doi: 10.1186/1471-2164-14-79424228734
102. Contrino S, Smith RN, Butano D, Carr A, Hu F, Lyne R, et al. modMine: flexible access to modENCODE data. Nucleic Acids Res. 2012;40: D1082–D1088. doi: 10.1093/nar/gkr92122080565
103. Brown JB, Boley N, Eisman R, May GE, Stoiber MH, Duff MO, et al. Diversity and dynamics of the Drosophila transcriptome. Nature. 2014;advance online publication. doi: 10.1038/nature12962
104. Guénin S, Mauriat M, Pelloux J, Wuytswinkel OV, Bellini C, Gutierrez L, Normalization of qRT-PCR data: the necessity of adopting a systematic, experimental conditions-specific, validation of references. J Exp Bot. 2009;60: 487–493. doi: 10.1093/jxb/ern30519264760
105. Hruz T, Wyss M, Docquier M, Pfaffl MW, Masanetz S, Borghi L, et al. RefGenes: identification of reliable and condition specific reference genes for RT-qPCR data normalization. BMC Genomics. 2011;12: 156. doi: 10.1186/1471-2164-12-15621418615
106. Graffelman J, Balding DJ, Gonzalez-Neira A, Bertranpetit J, Variation in estimated recombination rates across human populations. Hum Genet. 2007;122: 301–310. 17609980
107. Broman KW, Murray JC, Sheffield VC, White RL, Weber JL, Comprehensive human genetic maps: individual and sex-specific variation in recombination. Am J Hum Genet. 1998;63: 861–869. 9718341
108. Kohl KP, Jones CD, Sekelsky J, Evolution of an MCM complex in flies that promotes meiotic crossovers by blocking BLM helicase. Science. 2012;338: 1363–1365. doi: 10.1126/science.122819023224558
109. Fledel-Alon A, Wilson DJ, Broman K, Wen X, Ober C, Coop G, et al. Broad-scale recombination patterns underlying proper disjunction in humans. PLoS Genet. 2009;5: e1000658. doi: 10.1371/journal.pgen.100065819763175
110. Coop G, Wen X, Ober C, Pritchard JK, Przeworski M, High-resolution mapping of crossovers reveals extensive variation in fine-scale recombination patterns among humans. Science. 2008;319: 1395–1398. doi: 10.1126/science.115185118239090
111. Hadad RG, Pfeiffer TW, Poneleit CG, Repeatability and heritability of divergent recombination frequencies in the Iowa Stiff Stalk Synthetic (Zea mays L.). Theor Appl Genet. 1996;93: 990–996. doi: 10.1007/BF0022410324162435
112. Dewees AA, Genetic modification of recombination rate in Tribolium castaneum. Genetics. 1975;81: 537–552. 1205134
113. Shaw DD, Genetic and environmental components of chiasma control. II. The response to selection in Schistocerca. Chromosoma. 1972;37: 297–308. doi: 10.1007/BF003198725047774
114. Valentin J, Heritability of recombination frequency. Hereditas. 1973;75: 1–4. doi: 10.1111/j.1601-5223.1973.tb01136.x4204893
115. Plough HH, The effect of temperature on crossingover in Drosophila. J Exp Zool. 1917;24: 147–209.
116. Plough HH, Further studies on the effect of temperature on crossing over. J Exp Zool. 1921;32: 187–202.
117. Stern C, An effect of temperature and age on crossing-over in the first chromosome of Drosophila melanogaster. Genetics. 1926;12: 530–532.
118. Smith HF, Influence of temperature on crossing-over in Drosophila. Nature. 1936;138: 329–330.
119. Grell RF, Chandley AC, Evidence bearing on the coincidence of exchange and DNA replication in the oöcyte of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1965;53: 1340–1346. 5217635
120. Grell RF, The meiotic origin of temperature-induced crossovers in Drosophila melanogaster females. Genetics. 1966;54: 411–421. 17248319
121. Grushko TA, Korochkina SE, Klimenko VV, Temperature control of the crossing-over frequency in Drosophila melanogaster. Effect of infra- and super-optimal shock temperatures in early ontogenesis on the recombination frequency. Genetika. 1991;27: 1714–1721. 1778450
122. Jackson S, Nielsen DM, Singh ND, Increased exposure to acute thermal stress is associated with a non-linear increase in recombination frequency and an independent linear decrease in fitness in Drosophila. BMC Evol Biol. 2015;15: 175. doi: 10.1186/s12862-015-0452-826310872
123. Bridges CB, A linkage variation in Drosophila. J Exp Zool. 1915;19: 1–21.
124. Bridges CB, The relation of the age of the female to crossing over in the third chromosome of Drosophila melanogaster. J Gen Physiol. 1927;8: 689–700. 19872223
125. Bridges CB, Variation in crossing over in relation to the age of the female in Drosophila melanogaster. Carnegie Inst Wash. 1929;399: 63–89.
126. Bergner AD, The effect of prolongation of each stage of the life-cycle on crossing over in the second and third chromosomes of Drosophila melanogaster. J Exp Zool. 1928;50: 107–163.
127. Neel JV, A relation between larval nutrition and the frequency of crossing over in the third chromosome of Drosophila melanogaster. Genetics. 1941;26: 506–516. 17247020
128. Hayman DL, Parsons PA, The effect of temperature, age and an inversion on recombination values and interference in the X-chromosome of Drosophila melanogaster. Genetica. 1960;32: 74–88.
129. Redfield H, Delayed mating and relationship of recombination to maternal age in Drosophila melanogaster. Genetics. 1966;53: 593–607. 5919332
130. Lake S, Cederberg H, Recombination in females carrying a homozygous inverted X-chromosome in an inbred line of Drosophila melanogaster. Hereditas. 1984;10: 79–84.
131. Chadov BF, Chadova EV, Anan’ina GN, Kopyl SA, Volkova EI, Age-related changes in crossing over in Drosophila resemble the picture of interchromosomal effect of chromosome rearrangement on crossing over. Genetika. 2000;36: 331–338. 10779907
132. Priest NK, Roach DA, Galloway LF, Mating-induced recombination in fruit flies. Evolution. 2007; 160–167. 17300435
133. Tedman-Aucoin K, Agrawal AF, The effect of deleterious mutations and age on recombination in Drosophila melanogaster. Evolution. 2011;66: 575–585. doi: 10.1111/j.1558-5646.2011.01450.x22276549
134. Singh ND, Criscoe DR, Skolfield S, Kohl KP, Keebaugh ES, Schlenke TA, Fruit flies diversify their offspring in response to parasite infection. Science. 2015;349: 747–750. doi: 10.1126/science.aab176826273057
135. Werren JH, Biology of Wolbachia. Annu Rev Entomol. 1997;42: 587–609. doi: 10.1146/annurev.ento.42.1.58715012323
136. Jeyaprakash A, Hoy MA, Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Mol Biol. 2000;9: 393–405. doi: 10.1046/j.1365-2583.2000.00203.x10971717
137. Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH, How many species are infected with Wolbachia?–A statistical analysis of current data. FEMS Microbiol Lett. 2008;281: 215–220. doi: 10.1111/j.1574-6968.2008.01110.x18312577
138. Zug R, Hammerstein P, Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS ONE. 2012;7: e38544. doi: 10.1371/journal.pone.003854422685581
139. Clark ME, Anderson CL, Cande J, Karr TL, Widespread prevalence of Wolbachia in laboratory stocks and the implications for Drosophila research. Genetics. 2005;170: 1667–1675. doi: 10.1534/genetics.104.03890115937134
140. Richardson MF, Weinert LA, Welch JJ, Linheiro RS, Magwire MM, Jiggins FM, et al. Population genomics of the Wolbachia endosymbiont in Drosophila melanogaster. PLoS Genet. 2012;8: e1003129. doi: 10.1371/journal.pgen.100312923284297
141. Dobson SL, Bourtzis K, Braig HR, Jones BF, Zhou W, Rousset F, et al. Wolbachia infections are distributed throughout insect somatic and germ line tissues. Insect Biochem Mol Biol. 1999;29: 153–160. doi: 10.1016/S0965-1748(98)00119-210196738
142. Clark ME, Karr TL, Distribution of Wolbachia within Drosophila reproductive tissue: implications for the expression of cytoplasmic incompatibility. Integr Comp Biol. 2002;42: 332–339. doi: 10.1093/icb/42.2.33221708726
143. Hoffmann AA, Turelli M, Harshman LG, Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans. Genetics. 1990;126: 933–948. 2076821
144. Serga SV, Demidov SV, Kozeretska IA, Infection with Wolbachia does not influence crossing-over in Drosophila melanogaster. Cytol Genet. 2010;44: 239–243. doi: 10.3103/S0095452710040092
145. Dembeck LM, Huang W, Magwire MM, Lawrence F, Lyman RF, Mackay TFC, Genetic architecture of abdominal pigmentation in Drosophila melanogaster. PLoS Genet. 2015;11: e1005163. doi: 10.1371/journal.pgen.100516325933381
146. McKim KS, Jang JK, Manheim EA, Meiotic recombination and chromosome segregation in Drosophila females. Annu Rev Genet. 2002;36: 205–232. 12429692
147. Lake CM, Nielsen RJ, Hawley RS, The Drosophila zinc finger protein Trade Embargo is required for double strand break formation in meiosis. PLoS Genet. 2011;7: 1–15.
148. Huang W, Richards S, Carbone MA, Zhu D, Anholt RRH, Ayroles JF, et al. Epistasis dominates the genetic architecture of Drosophila quantitative traits. Proc Natl Acad Sci. 2012;109: 15553–15559. doi: 10.1073/pnas.121342310922949659
149. Mackay TFC, Epistasis and quantitative traits: using model organisms to study gene-gene interactions. Nat Rev Genet. 2013;advance online publication.
150. Döring F, Scholz H, Kühnlein RP, Karschin A, Wischmeyer E, Novel Drosophila two-pore domain K+ channels: rescue of channel function by heteromeric assembly. Eur J Neurosci. 2006;24: 2264–2274. doi: 10.1111/j.1460-9568.2006.05102.x17074048
151. Pàldi A, Gyapay G, Jami J, Imprinted chromosomal regions of the human genome display sex-specific meiotic recombination frequencies. Curr Biol. 1995;5: 1030–1035. doi: 10.1016/S0960-9822(95)00207-78542279
152. Coolon JD, Stevenson KR, McManus CJ, Graveley BR, Wittkopp PJ, Genomic imprinting absent in Drosophila melanogaster adult females. Cell Rep. 2012;2: 69–75. doi: 10.1016/j.celrep.2012.06.01322840398
153. Konola JT, Logan KM, Knight KL, Functional characterization of residues in the P-loop motif of the RecA protein ATP binding site. J Mol Biol. 1994;237: 20–34. doi: 10.1006/jmbi.1994.12068133517
154. Dresser ME, Ewing DJ, Conrad MN, Dominguez AM, Barstead R, Jiang H, et al. DMC1 functions in a Saccharomyces cerevisiae meiotic pathway that is largely independent of the RAD51 pathway. Genetics. 1997;147: 533–544. 9335591
155. Shinohara A, Ogawa H, Ogawa T, Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell. 1992;69: 457–470. doi: 10.1016/0092-8674(92)90447-K1581961
156. Johnson RD, Symington LS, Functional differences and interactions among the putative RecA homologs Rad51, Rad55, and Rad57. Mol Cell Biol. 1995;15: 4843–4850. 7651402
157. Rafii S, Lindblom A, Reed M, Meuth M, Cox A, A naturally occurring mutation in an ATP-binding domain of the recombination repair gene XRCC3 ablates its function without causing cancer susceptibility. Hum Mol Genet. 2003;12: 915–923. doi: 10.1093/hmg/ddg10212668615
158. Morris LX, Spradling AC, Steroid signaling within Drosophila ovarian epithelial cells sex-specifically modulates early germ cell development and meiotic entry. PLoS ONE. 2012;7: e46109. doi: 10.1371/journal.pone.004610923056242
159. Garen A, Kauvar L, Lepesant J-A, Roles of ecdysone in Drosophila development. Proc Natl Acad Sci. 1977;74: 5099–5103. 16592466
160. Bownes M, Blair M, Kozma R, Dempster M, 20-hydroxyecdysone stimulates tissue-specific yolk-protein gene transcription in both male and female Drosophila. J Embryol Exp Morphol. 1983;78: 249–268. 6198419
161. Gaziova I, Bonnette PC, Henrich VC, Jindra M, Cell-autonomous roles of the ecdysoneless gene in Drosophila development and oogenesis. Development. 2004;131: 2715–2725. doi: 10.1242/dev.0114315128659
162. Morgan TH, Complete linkage in the second chromosome of the male of Drosophila. Science. 1912;36: 719–720.
163. Morgan TH, No crossing over in the male of Drosophila of genes in the second and third pairs of chromosomes. Biol Bull. 1914;26: 195–204.
164. Seeger M, Tear G, Ferres-Marco D, Goodman CS, Mutations affecting growth cone guidance in Drosophila: genes necessary for guidance toward or away from the midline. Neuron. 1993;10: 409–426. doi: 10.1016/0896-6273(93)90330-T8461134
165. Giniger E, Tietje K, Jan LY, Jan YN, lola encodes a putative transcription factor required for axon growth and guidance in Drosophila. Development. 1994;120: 1385–1398. 8050351
166. Shin EJ, Shin HM, Nam E, Kim WS, Kim J-H, Oh B-H, et al. DeSUMOylating isopeptidase: a second class of SUMO protease. EMBO Rep. 2012;13: 339–346. doi: 10.1038/embor.2012.322370726
167. Potts PR, The yin and yang of the MMS21–SMC5/6 SUMO ligase complex in homologous recombination. DNA Repair. 2009;8: 499–506. doi: 10.1016/j.dnarep.2009.01.00919217832
168. Baeg G-H, Zhou R, Perrimon N, Genome-wide RNAi analysis of JAK/STAT signaling components in Drosophila. Genes Dev. 2005;19: 1861–1870. doi: 10.1101/gad.132070516055650
169. Müller P, Kuttenkeuler D, Gesellchen V, Zeidler MP, Boutros M, Identification of JAK/STAT signalling components by genome-wide RNA interference. Nature. 2005;436: 871–875. 16094372
170. Ursuliak Z, Clemens JC, Dixon JE, Price JV, Differential accumulation of DPTP61F alternative transcripts: regulation of a protein tyrosine phosphatase by segmentation genes. Mech Dev. 1997;65: 19–30. 9256342
171. Fitzpatrick KA, Gorski SM, Ursuliak Z, Price JV, Expression of protein tyrosine phosphatase genes during oogenesis in Drosophila melanogaster. Mech Dev. 1995;53: 171–183. doi: 10.1016/0925-4773(95)00432-Z8562420
172. Buszard BJ, Johnson TK, Meng T-C, Burke R, Warr CG, Tiganis T, The nucleus- and endoplasmic reticulum-targeted forms of Protein Tyrosine Phosphatase 61F regulate Drosophila growth, life span, and fecundity. Mol Cell Biol. 2013;33: 1345–1356. doi: 10.1128/MCB.01411-1223339871
173. Través PG, Pardo V, Pimentel-Santillana M, González-Rodríguez Á, Mojena M, Rico D, et al. Pivotal role of protein tyrosine phosphatase 1B (PTP1B) in the macrophage response to pro-inflammatory and anti-inflammatory challenge. Cell Death Dis. 2014;5: e1125. doi: 10.1038/cddis.2014.9024625984
174. Lyman RF, Lawrence F, Nuzhdin SV, Mackay TFC, Effects of single P-Element insertions on bristle number and viability in Drosophila melanogaster. Genetics. 1996;143: 277–292. 8722781
175. Turner SD, qqman: an R package for visualizing GWAS results using Q-Q and manhattan plots. bioRxiv. 2014; 005165. doi: 10.1101/005165
176. Van Doren M, Williamson AL, Lehmann R, Regulation of zygotic gene expression in Drosophila primordial germ cells. Curr Biol. 1998;8: 243–246. doi: 10.1016/S0960-9822(98)70091-09501989
177. Rørth P, Gal4 in the Drosophila female germline. Mech Dev. 1998;78: 113–118. doi: 10.1016/S0925-4773(98)00157-99858703
178. Wang C, Dickinson LK, Lehmann R, Genetics of nanos localization in Drosophila. Dev Dyn. 1994;199: 103–115. doi: 10.1002/aja.10019902047515724
179. Dunnett CW, A multiple comparison procedure for comparing several treatments with a control. J Am Stat Assoc. 1955;50: 1096–1121. doi: 10.2307/2281208
180. Dunnett CW, New tables for multiple comparisons with a control. Biometrics. 1964;20: 482–491.
181. Hu Y, Sopko R, Foos M, Kelley C, Flockhart I, Ammeux N, et al. FlyPrimerBank: an online database for Drosophila melanogaster gene expression analysis and knockdown evaluation of RNAi reagents. G3 GenesGenomesGenetics. 2013;3: 1607–1616. doi: 10.1534/g3.113.007021
182. Suzuki T, Higgins PJ, Crawford DR, Control selection for RNA quantitation. BioTechniques. 2000;29: 332–337. 10948434
183. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002;3: research0034.1–research0034.11.