1932

Abstract

Through recombination, genes are freed to evolve more independently of one another, unleashing genetic variance hidden in the linkage disequilibrium that accumulates through selection combined with drift. Yet crossover numbers are evolutionarily constrained, with at least one and not many more than one crossover per bivalent in most taxa. Crossover interference, whereby a crossover reduces the probability of a neighboring crossover, contributes to this homogeneity. The mechanisms by which interference is achieved and crossovers are regulated are a major current subject of inquiry, facilitated by novel methods to visualize crossovers and to pinpoint recombination events. Here, we review patterns of crossover interference and the models built to describe this process. We then discuss the selective forces that have likely shaped interference and the regulation of crossover numbers.

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2019-12-03
2024-12-02
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Literature Cited

  1. 1. 
    Aggarwal DD, Rashkovetsky E, Michalak P, Cohen I, Ronin Y et al. 2015. Experimental evolution of recombination and crossover interference in Drosophila caused by directional selection for stress-related traits. BMC Biol 13:101
    [Google Scholar]
  2. 2. 
    Altenberg L, Feldman MW. 1987. Selection, generalized transmission and the evolution of modifier genes. I. The reduction principle. Genetics 117:559–72
    [Google Scholar]
  3. 3. 
    Anderson CM, Oke A, Yam P, Zhuge T, Fung JC 2015. Reduced crossover interference and increased ZMM-independent recombination in the absence of Tel1/ATM. PLOS Genet 11:e1005478
    [Google Scholar]
  4. 4. 
    Anderson LK, Doyle GG, Brigham B, Carter J, Hooker KD et al. 2003. High-resolution crossover maps for each bivalent of Zea mays using recombination nodules. Genetics 165:849–65
    [Google Scholar]
  5. 5. 
    Anderson LK, Hooker KD, Stack SM 2001. The distribution of early recombination nodules on zygotene bivalents from plants. Genetics 159:1259–69
    [Google Scholar]
  6. 6. 
    Anderson LK, Lohmiller LD, Tang X, Hammond DB, Javernick L et al. 2014. Combined fluorescent and electron microscopic imaging unveils the specific properties of two classes of meiotic crossovers. PNAS 111:13415–20
    [Google Scholar]
  7. 7. 
    Barakate A, Higgins JD, Vivera S, Stephens J, Perry RM et al. 2014. The synaptonemal complex protein ZYP1 is required for imposition of meiotic crossovers in barley. Plant Cell 26:729–40
    [Google Scholar]
  8. 8. 
    Barlow AL, Benson FE, West SC, Hultén MA 1997. Distribution of the Rad51 recombinase in human and mouse spermatocytes. EMBO J 16:5207–15
    [Google Scholar]
  9. 9. 
    Barlow AL, Hultén MA. 1998. Crossing over analysis at pachytene in man. Eur. J. Hum. Genet. 6:350–58
    [Google Scholar]
  10. 10. 
    Barton NH. 1995. A general model for the evolution of recombination. Genet. Res. 65:123–45
    [Google Scholar]
  11. 11. 
    Barton NH, Otto SP. 2005. Evolution of recombination due to random drift. Genetics 169:2353–70
    [Google Scholar]
  12. 12. 
    Basheva EA, Bidau CJ, Borodin PM 2008. General pattern of meiotic recombination in male dogs estimated by MLH1 and RAD51 immunolocalization. Chromosome Res 16:709–19
    [Google Scholar]
  13. 13. 
    Basu-Roy S, Gauthier F, Giraut L, Mézard C, Falque M, Martin OC 2013. Hot regions of noninterfering crossovers coexist with a nonuniformly interfering pathway in Arabidopsis thaliana. Genetics 195:769–79
    [Google Scholar]
  14. 14. 
    Bauer E, Falque M, Walter H, Bauland C, Camisan C et al. 2013. Intraspecific variation of recombination rate in maize. Genome Biol 14:R103–17
    [Google Scholar]
  15. 15. 
    Bell G. 1982. The Masterpiece of Nature: The Genetics and Evolution of Sexuality Berkeley: University of California Press
    [Google Scholar]
  16. 16. 
    Berchowitz LE, Copenhaver GP. 2010. Genetic interference: Don't stand so close to me. Curr. Genom. 11:91–102
    [Google Scholar]
  17. 17. 
    Borodin PM, Basheva EA, Zhelezova AI 2009. Immunocytological analysis of meiotic recombination in the American mink (Mustela vison). Anim. Genet. 40:235–38
    [Google Scholar]
  18. 18. 
    Borodin PM, Karamysheva TV, Belonogova NM, Torgasheva AA, Rubtsov NB, Searle JB 2008. Recombination map of the common shrew, Sorex araneus (Eulipotyphla, Mammalia). Genetics 178:621–32
    [Google Scholar]
  19. 19. 
    Borodin PM, Karamysheva TV, Rubtsov NB 2007. Immunofluorescent analysis of meiotic recombination in the domestic cat. Cell Tiss. Biol. 1:503–7
    [Google Scholar]
  20. 20. 
    Brady MM, McMahan S, Sekelsky J 2018. Loss of Drosophila Mei-41/ATR alters meiotic crossover patterning. Genetics 208:579–88
    [Google Scholar]
  21. 21. 
    Brandvain Y, Coop G. 2012. Scrambling eggs: meiotic drive and the evolution of female recombination rates. Genetics 190:709–23
    [Google Scholar]
  22. 22. 
    Bridges CB. 1916. Non-disjunction as proof of the chromosome theory of heredity (concluded). Genetics 1:107–63
    [Google Scholar]
  23. 23. 
    Campbell CL, Bhérer C, Morrow BE, Boyko AR, Auton A 2016. pedigree-based map of recombination in the domestic dog genome. Genes Genom. Genet. 6:3517–24
    [Google Scholar]
  24. 24. 
    Campbell CL, Furlotte NA, Eriksson N, Hinds D, Auton A 2015. Escape from crossover interference increases with maternal age. Nat. Commun. 6:6260
    [Google Scholar]
  25. 25. 
    Chakraborty P, Pankajam AV, Lin G, Dutta A, Krishnaprasad GN et al. 2017. Modulating crossover frequency and interference for obligate crossovers in Saccharomyces cerevisiae meiosis. Genes Genom. Genet 7:1511–24
    [Google Scholar]
  26. 26. 
    Charlesworth B, Charlesworth D. 1985. Genetic variation in recombination in Drosophila. I. Responses to selection and preliminary genetic analysis. Heredity 54:71–83
    [Google Scholar]
  27. 27. 
    Cobbs G. 1978. Renewal process approach to the theory of genetic linkage: case of no chromatid interference. Genetics 89:563–81
    [Google Scholar]
  28. 28. 
    Cole F, Kauppi L, Lange J, Roig I, Wang R et al. 2012. Homeostatic control of recombination is implemented progressively in mouse meiosis. Nat. Cell Biol. 14:424–30
    [Google Scholar]
  29. 29. 
    Cole F, Keeney S, Jasin M 2010. Comprehensive, fine-scale dissection of homologous recombination outcomes at a hot spot in mouse meiosis. Mol. Cell 39:700–10
    [Google Scholar]
  30. 30. 
    Comeron JM, Ratnappan R, Bailin S 2012. The many landscapes of recombination in Drosophila melanogaster. PLOS Genet 8:e1002905
    [Google Scholar]
  31. 31. 
    Conrad DF, Keebler JEM, DePristo MA, Lindsay SJ, Zhang Y et al. 2011. Variation in genome-wide mutation rates within and between human families. Nat. Genet. 43:712–14
    [Google Scholar]
  32. 32. 
    Cooper TJ, Crawford MR, Hunt LJ, Marsolier-Kergoat M-C, Llorente B, Neale MJ 2018. Mismatch repair impedes meiotic crossover interference. bioRxiv 480418. https://doi.org/10.1101/480418
    [Crossref]
  33. 33. 
    Copenhaver GP, Housworth EA, Stahl FW 2002. Crossover interference in Arabidopsis. Genetics 160:1631–39
    [Google Scholar]
  34. 34. 
    Crow JF. 1970. Genetic loads and the cost of natural selection. Mathematical Topics in Population Genetics K-I Kojima 128–77 New York: Springer-Verlag
    [Google Scholar]
  35. 35. 
    de Boer E, Stam P, Dietrich AJJ, Pastink A, Heyting C 2006. Two levels of interference in mouse meiotic recombination. PNAS 103:9607–12
    [Google Scholar]
  36. 36. 
    de los Santos T, Hunter N, Lee C, Larkin B, Loidl J, Hollingsworth NM 2003. The Mus81/Mms4 endonuclease acts independently of double-Holliday junction resolution to promote a distinct subset of crossovers during meiosis in budding yeast. Genetics 164:81–94
    [Google Scholar]
  37. 37. 
    Dreissig S, Fuchs J, Himmelbach A, Mascher M, Houben A 2017. Sequencing of single pollen nuclei reveals meiotic recombination events at megabase resolution and circumvents segregation distortion caused by postmeiotic processes. Front. Plant Sci. 8:1620
    [Google Scholar]
  38. 38. 
    Dunce JM, Milburn AE, Gurusaran M, Cruz I, Sen LT et al. 2019. Structural basis of meiotic telomere attachment to the nuclear envelope by MAJIN-TERB2-TERB1. Nat. Commun. 9:5355
    [Google Scholar]
  39. 39. 
    Falque M, Anderson LK, Stack SM, Gauthier F, Martin OC 2009. Two types of meiotic crossovers coexist in maize. Plant Cell 21:3915–25
    [Google Scholar]
  40. 40. 
    Falque M, Mercier R, Mézard C, de Vienne D, Martin OC 2007. Patterns of recombination and MLH1 foci density along mouse chromosomes: modeling effects of interference and obligate chiasma. Genetics 176:1453–67
    [Google Scholar]
  41. 41. 
    Foss EJ, Lande R, Stahl FW, Steinberg CM 1993. Chiasma interference as a function of genetic distance. Genetics 133:681–91
    [Google Scholar]
  42. 42. 
    Foss EJ, Stahl FW. 1995. A test of a counting model for chiasma interference. Genetics 139:1201–9
    [Google Scholar]
  43. 43. 
    Fowler KR, Hyppa RW, Cromie GA, Smith GR 2018. Physical basis for long-distance communication along meiotic chromosomes. PNAS 115:E9333–42
    [Google Scholar]
  44. 44. 
    Ganetzky B, Hawley RS. 2016. The centenary of GENETICS: bridges to the future. Genetics 202:15–23
    [Google Scholar]
  45. 45. 
    Garcia V, Gray S, Allison RM, Cooper TJ, Neale MJ 2015. Tel1ATM-mediated interference suppresses clustered meiotic double-strand-break formation. Nature 520:114–18
    [Google Scholar]
  46. 46. 
    Giraut L, Falque M, Drouaud J, Pereira L, Martin OC, Mézard C 2011. Genome-wide crossover distribution in Arabidopsis thaliana meiosis reveals sex-specific patterns along chromosomes. PLOS Genet 7:e1002354
    [Google Scholar]
  47. 47. 
    Goldstein DB, Bergman A, Feldman MW 1993. The evolution of interference: reduction of recombination among three loci. Theor. Popul. Biol. 44:246–59
    [Google Scholar]
  48. 48. 
    Gray S, Cohen PE. 2016. Control of meiotic crossovers: from double-strand break formation to designation. Annu. Rev. Genet. 50:175–210
    [Google Scholar]
  49. 49. 
    Gruhn JR, Rubio C, Broman KW, Hunt PA, Hassold T 2013. Cytological studies of human meiosis: sex-specific differences in recombination originate at, or prior to, establishment of double-strand breaks. PLOS ONE 8:e85075
    [Google Scholar]
  50. 50. 
    Haenel Q, Laurentino TG, Roesti M, Berner D 2018. Meta-analysis of chromosome-scale crossover rate variation in eukaryotes and its significance to evolutionary genomics. Mol. Ecol. 27:2477–97
    [Google Scholar]
  51. 51. 
    Haldane J. 1919. The combination of linkage values and the calculation of distances between the loci. J. Genet. 8:299–309
    [Google Scholar]
  52. 52. 
    Halldorsson BV, Palsson G, Stefansson OA, Jonsson H, Hardarson MT et al. 2019. Characterizing mutagenic effects of recombination through a sequence-level genetic map. Science 363:eaau1043
    [Google Scholar]
  53. 53. 
    Hassold T, Hunt P. 2001. To err (meiotically) is human: the genesis of human aneuploidy. Nat. Rev. Genet. 2:280–91
    [Google Scholar]
  54. 54. 
    Hatkevich T, Kohl KP, McMahan S, Hartmann MA, Williams AM, Sekelsky J 2017. Bloom syndrome helicase promotes meiotic crossover patterning and homolog disjunction. Curr. Biol. 27:96–102
    [Google Scholar]
  55. 55. 
    Hollingsworth NM, Brill SJ. 2004. The Mus81 solution to resolution: generating meiotic crossovers without Holliday junctions. Genes Dev 18:117–25
    [Google Scholar]
  56. 56. 
    Housworth EA, Stahl FW. 2003. Crossover interference in humans. Am. J. Hum. Genet. 73:188–97
    [Google Scholar]
  57. 57. 
    Hughes SE, Miller DE, Miller AL, Hawley RS 2018. Female meiosis: synapsis, recombination, and segregation in Drosophila melanogaster. Genetics 208:875–908
    [Google Scholar]
  58. 58. 
    Hunter N. 2015. Meiotic recombination: the essence of heredity. Cold Spring Harb. Perspect. Biol. 7:a016618
    [Google Scholar]
  59. 59. 
    International Human Genome Sequencing Consortium 2004. Finishing the euchromatic sequence of the human genome. Nature 431:931–45
    [Google Scholar]
  60. 60. 
    Ioannou D, Fortun J, Tempest HG 2018. Meiotic nondisjunction and sperm aneuploidy in humans. Reproduction 157:R15–31
    [Google Scholar]
  61. 61. 
    Ito M, Kugou K, Fawcett JA, Mura S, Ikeda S et al. 2014. Meiotic recombination cold spots in chromosomal cohesion sites. Genes Cells 19:359–73
    [Google Scholar]
  62. 62. 
    Jeffreys AJ, May CA. 2004. Intense and highly localized gene conversion activity in human meiotic crossover hot spots. Nat. Genet. 36:151–56
    [Google Scholar]
  63. 63. 
    Jessop L, Rockmill B, Roeder GS, Lichten M 2006. Meiotic chromosome synapsis-promoting proteins antagonize the anti-crossover activity of Sgs1. PLOS Genet 2:e155
    [Google Scholar]
  64. 64. 
    Kauppi L, Barchi M, Lange J, Baudat F, Jasin M, Keeney S 2013. Numerical constraints and feedback control of double-strand breaks in mouse meiosis. Genes Dev 27:873–86
    [Google Scholar]
  65. 65. 
    Kauppi L, Jasin M, Keeney S 2014. How much is enough? Control of DNA double-strand break numbers in mouse meiosis. Cell Cycle 12:2719–20
    [Google Scholar]
  66. 66. 
    Keightley PD, Otto SP. 2006. Interference among deleterious mutations favours sex and recombination in finite populations. Nature 443:89–92
    [Google Scholar]
  67. 67. 
    King JS, Mortimer RK. 1990. A polymerization model of chiasma interference and corresponding computer simulation. Genetics 126:1127–38
    [Google Scholar]
  68. 68. 
    Kleckner N. 2016. Questions and assays. Genetics 204:1343–49
    [Google Scholar]
  69. 69. 
    Kleckner N, Zickler D, Jones GH, Dekker J, Padmore R et al. 2004. A mechanical basis for chromosome function. PNAS 101:12592–97
    [Google Scholar]
  70. 70. 
    Koehler KE, Boulton CL, Collins HE, French RL, Herman KC et al. 1996. Spontaneous X chromosome MI and MII nondisjunction events in Drosophila melanogaster oocytes have different recombinational histories. Nat. Genet. 14:406–14
    [Google Scholar]
  71. 71. 
    Koehler KE, Cherry JP, Lynn A, Hunt PA, Hassold TJ 2002. Genetic control of mammalian meiotic recombination. I. Variation in exchange frequencies among males from inbred mouse strains. Genetics 162:297–306
    [Google Scholar]
  72. 72. 
    Koehler KE, Hawley RS, Sherman S, Hassold T 1996. Recombination and nondisjunction in humans and flies. Hum. Mol. Genet. 5:1495–504
    [Google Scholar]
  73. 73. 
    Kosambi DD. 1944. The estimation of map distances from recombination values. Ann. Eugen. 12:172–75
    [Google Scholar]
  74. 74. 
    Krishnaprasad GN, Anand MT, Lin G, Tekkedil MM, Steinmetz LM, Nishant KT 2015. Variation in crossover frequencies perturb crossover assurance without affecting meiotic chromosome segregation in Saccharomyces cerevisiae. Genetics 199:399–412
    [Google Scholar]
  75. 75. 
    Kurdzo EL, Chuong HH, Evatt JM, Dawson DS 2018. A ZIP1 separation-of-function allele reveals that centromere pairing drives meiotic segregation of achiasmate chromosomes in budding yeast. PLOS Genet 14:e1007513
    [Google Scholar]
  76. 76. 
    Lenormand T, Dutheil J. 2005. Recombination difference between sexes: a role for haploid selection. PLOS Biol 3:e63
    [Google Scholar]
  77. 77. 
    Limborg MT, Waples RK, Allendorf FW, Seeb JE 2015. Linkage mapping reveals strong chiasma interference in sockeye salmon: implications for interpreting genomic data. Genes Genom. Genet. 5:2463–73
    [Google Scholar]
  78. 78. 
    Lisachov AP, Tishakova KV, Tsepilov YA, Borodin PM 2019. Male meiotic recombination in the steppe agama, Trapelus sanguinolentus (Agamidae, Iguania, Reptilia). Cytogenet. Genome Res. 157:107–14
    [Google Scholar]
  79. 79. 
    Lisachov AP, Trifonov VA, Giovannotti M, Ferguson-Smith MA, Borodin PM 2017. Immunocytological analysis of meiotic recombination in two anole lizards (Squamata, Dactyloidae). Comp. Cytogenet. 11:129–41
    [Google Scholar]
  80. 80. 
    Lloyd A, Jenczewski E. 2019. Modelling sex-specific crossover patterning in Arabidopsis. Genetics 211:847–59
    [Google Scholar]
  81. 81. 
    Machovina TS, Mainpal R, Daryabeigi A, McGovern O, Paouneskou D et al. 2016. A surveillance system ensures crossover formation in C. elegans. Curr. Biol 26:2873–84
    [Google Scholar]
  82. 82. 
    Maguire MP. 1980. Adaptive advantage for chiasma interference: a novel suggestion. Heredity 45:127–31
    [Google Scholar]
  83. 83. 
    Mancera E, Bourgon R, Brozzi A, Huber W, Steinmetz LM 2008. High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454:479–85
    [Google Scholar]
  84. 84. 
    Marsolier-Kergoat MC, Khan MM, Schott J, Zhu X, Llorente B 2018. Mechanistic view and genetic control of DNA recombination during meiosis. Mol. Cell 70:9–20.e6
    [Google Scholar]
  85. 85. 
    McPeek MS, Speed TP. 1995. Modeling interference in genetic recombination. Genetics 139:1031–44
    [Google Scholar]
  86. 86. 
    Mehrotra S, McKim KS. 2006. Temporal analysis of meiotic DNA double-strand break formation and repair in Drosophila females. PLOS Genet 2:e200
    [Google Scholar]
  87. 87. 
    Miller DE, Smith CB, Kazemi NY, Cockrell AJ, Arvanitakas AV et al. 2016. Whole-genome analysis of individual meiotic events in Drosophila melanogaster reveals that noncrossover gene conversions are insensitive to interference and the centromere effect. Genetics 203:159–71
    [Google Scholar]
  88. 88. 
    Muller HJ. 1916. The mechanism of crossing-over. Am. Nat. 50:193–221
    [Google Scholar]
  89. 89. 
    Munz P. 1994. An analysis of interference in the fission yeast Schizosaccharomyces pombe. Genetics 137:701–7
    [Google Scholar]
  90. 90. 
    Nagaoka SI, Hassold TJ, Hunt PA 2012. Human aneuploidy: mechanisms and new insights into an age-old problem. Nat. Publ. Group 13:493–504
    [Google Scholar]
  91. 91. 
    Nilsson N-O, Säll T. 1995. A model of chiasma reduction of closely formed crossovers. J. Theor. Biol. 173:93–98
    [Google Scholar]
  92. 92. 
    Otto SP. 2009. The evolutionary enigma of sex. Am. Nat. 174:Suppl. 1S1–14
    [Google Scholar]
  93. 93. 
    Otto SP, Barton NH. 2001. Selection for recombination in small populations. Evolution 55:1921–31
    [Google Scholar]
  94. 94. 
    Otto SP, Day T. 2007. A Biologist's Guide to Mathematical Modeling in Ecology and Evolution Princeton, NJ: Princeton Univ. Press
    [Google Scholar]
  95. 95. 
    Ottolini CS, Newnham LJ, Capalbo A, Natesan SA, Joshi HA et al. 2015. Genome-wide maps of recombination and chromosome segregation in human oocytes and embryos show selection for maternal recombination rates. Nat. Genet. 47:727–35
    [Google Scholar]
  96. 96. 
    Petkov PM, Broman KW, Szatkiewicz JP, Paigen K 2007. Crossover interference underlies sex differences in recombination rates. Trends Genet 23:539–42
    [Google Scholar]
  97. 97. 
    Pratto F, Brick K, Khil P, Smagulova F, Petukhova GV, Camerini-Otero RD 2014. DNA recombination. Recombination initiation maps of individual human genomes. Science 346:1256442
    [Google Scholar]
  98. 98. 
    Raffoux X, Bourge M, Dumas F, Martin OC, Falque M 2018. High-throughput measurement of recombination rates and genetic interference in Saccharomyces cerevisiae. Yeast 35:431–42
    [Google Scholar]
  99. 99. 
    Raffoux X, Bourge M, Dumas F, Martin OC, Falque M 2018. Role of cis, trans, and inbreeding effects on meiotic recombination in Saccharomyces cerevisiae. Genetics 210:1213–26
    [Google Scholar]
  100. 100. 
    Rattray A, Santoyo G, Shafer B, Strathern JN 2015. Elevated mutation rate during meiosis in Saccharomyces cerevisiae. PLOS Genet 11:e1004910
    [Google Scholar]
  101. 101. 
    Rockmill B, Fung JC, Branda SS, Roeder GS 2003. The Sgs1 helicase regulates chromosome synapsis and meiotic crossing over. Curr. Biol. 13:1954–62
    [Google Scholar]
  102. 102. 
    Rogers DW, McConnell E, Ono J, Greig D 2018. Spore-autonomous fluorescent protein expression identifies meiotic chromosome mis-segregation as the principal cause of hybrid sterility in yeast. PLOS Biol 16:e2005066
    [Google Scholar]
  103. 103. 
    Rosu S, Zawadzki KA, Stamper EL, Libuda DE, Reese AL et al. 2013. The C. elegans DSB-2 protein reveals a regulatory network that controls competence for meiotic DSB formation and promotes crossover assurance. PLOS Genet 9:e1003674
    [Google Scholar]
  104. 104. 
    Roze D, Barton NH. 2006. The Hill–Robertson effect and the evolution of recombination. Genetics 173:1793–811
    [Google Scholar]
  105. 105. 
    Ruiz-Herrera A, Vozdova M, Fernández J, Sebestova H, Capilla L et al. 2017. Recombination correlates with synaptonemal complex length and chromatin loop size in bovids—insights into mammalian meiotic chromosomal organization. Chromosoma 126:615–31
    [Google Scholar]
  106. 106. 
    Segura J, Ferretti L, Ramos-Onsins S, Capilla L, Farré M et al. 2013. Evolution of recombination in eutherian mammals: insights into mechanisms that affect recombination rates and crossover interference. Proc. R. Soc. B 280:20131945
    [Google Scholar]
  107. 107. 
    Sharp NP, Sandell L, James CG, Otto SP 2018. The genome-wide rate and spectrum of spontaneous mutations differ between haploid and diploid yeast. PNAS 115:E5046–55
    [Google Scholar]
  108. 108. 
    Sidhu GK, Fang C, Olson MA, Falque M, Martin OC, Pawlowski WP 2015. Recombination patterns in maize reveal limits to crossover homeostasis. PNAS 112:15982–87
    [Google Scholar]
  109. 109. 
    Smukowski CS, Noor MAF. 2011. Recombination rate variation in closely related species. Heredity 107:496–508
    [Google Scholar]
  110. 110. 
    Stadler DR. 1959. The relationship of gene conversion to crossing over in Neurospora. PNAS 45:1625–29
    [Google Scholar]
  111. 111. 
    Stam P. 1979. Interference in genetic crossing over and chromosome mapping. Genetics 92:573–94
    [Google Scholar]
  112. 112. 
    Stapley J, Feulner PGD, Johnston SE, Santure AW, Smadja CM 2017. Variation in recombination frequency and distribution across eukaryotes: patterns and processes. Philos. Trans. R. Soc. B 372:20160455
    [Google Scholar]
  113. 113. 
    Strathern JN, Shafer BK, McGill CB 1995. DNA synthesis errors associated with double-strand-break repair. Genetics 140:965–72
    [Google Scholar]
  114. 114. 
    Strickland WN. 1958. An analysis of interference in Aspergillus nidulans. Proc. R. Soc. B 149:82–101
    [Google Scholar]
  115. 115. 
    Sturtevant AH. 1913. The linear arrangement of six sex‐linked factors in Drosophila, as shown by their mode of association. J. Exp. Zool. 14:43–59
    [Google Scholar]
  116. 116. 
    Sturtevant AH. 1915. The behavior of the chromosomes as studied through linkage. Z. Indukt. Abstamm. Vererbung. 13:234–87
    [Google Scholar]
  117. 117. 
    Tessé S, Bourbon HM, Debuchy R, Budin K, Dubois E et al. 2017. Asy2/Mer2: an evolutionarily conserved mediator of meiotic recombination, pairing, and global chromosome compaction. Genes Dev 31:1880–93
    [Google Scholar]
  118. 118. 
    Torgasheva AA, Borodin PM. 2017. Immunocytological analysis of meiotic recombination in the gray goose (Anser anser). Cytogenet. Genome Res. 151:27–35
    [Google Scholar]
  119. 119. 
    Veller C, Kleckner N, Nowak MA 2019. A rigorous measure of genome-wide genetic shuffling that takes into account crossover positions and Mendel's second law. PNAS 116:1659–68
    [Google Scholar]
  120. 120. 
    Wang K, Wang M, Tang D, Shen Y, Miao C et al. 2012. The role of rice HEI10 in the formation of meiotic crossovers. PLOS Genet 8:e1002809
    [Google Scholar]
  121. 121. 
    Wang Z, Shen B, Jiang J, Li J, Ma L 2016. Effect of sex, age and genetics on crossover interference in cattle. Sci. Rep. 6:37698
    [Google Scholar]
  122. 122. 
    Weinstein A. 1918. Coincidence of crossing over in Drosophila melanogaster (ampelophila). Genetics 3:135–72
    [Google Scholar]
  123. 123. 
    Yue JX, Li J, Aigrain L, Hallin J, Persson K et al. 2017. Contrasting evolutionary genome dynamics between domesticated and wild yeasts. Nat. Genet. 49:913–24
    [Google Scholar]
  124. 124. 
    Zalevsky J, MacQueen AJ, Duffy JB, Kemphues KJ, Villeneuve AM 1999. Crossing over during Caenorhabditis elegans meiosis requires a conserved MutS-based pathway that is partially dispensable in budding yeast. Genetics 153:1271–83
    [Google Scholar]
  125. 125. 
    Zhang L, Liang Z, Hutchinson J, Kleckner N 2014. Crossover patterning by the beam-film model: analysis and implications. PLOS Genet 10:e1004042
    [Google Scholar]
  126. 126. 
    Zhang L, Wang S, Yin S, Hong S, Kim KP, Kleckner N 2014. Topoisomerase II mediates meiotic crossover interference. Nature 511:551–56
    [Google Scholar]
  127. 127. 
    Zhao H, Speed TP. 1996. On genetic map functions. Genetics 142:1369–77
    [Google Scholar]
  128. 128. 
    Zickler D. 2006. From early homologue recognition to synaptonemal complex formation. Chromosoma 115:158–74
    [Google Scholar]
  129. 129. 
    Zickler D, Kleckner N. 2015. Recombination, pairing, and synapsis of homologs during meiosis. Cold Spring Harb. Perspect. Biol. 7:a016626
    [Google Scholar]
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