Recombination Rates in Drosophila

Abstract

Recombination occurs during meiosis to produce new allelic combinations in natural populations, making it important for studying evolution. The model system Drosophila has been crucial for understanding the mechanics underlying recombination and assessing the association between recombination rate and several evolutionary parameters. Drosophila was the first system in which genetic maps were developed using recombination frequencies between genes. Linkage maps have been subsequently developed in many biological systems, including humans. Fungal systems have been helpful in highlighting the mechanics of recombination and identifying particular enzymes that perform various steps in the process; however, similar proteins have been identified in Drosophila. Further, Drosophila has been used to determine genetic and environmental conditions that cause variation in recombination rate. Finally, Drosophila has been instrumental in elucidating associations between local recombination rate and nucleotide diversity, divergence and codon bias, as well as helping determine the causes of these associations.

Key Concepts

  • Recombination refers to either independent assortment or crossing over, both of which are responsible for introducing genetic variation during meiosis.

  • Drosophila has been crucial in the development of genetic mapping techniques, which have been extended to other organismal systems including humans.

  • Fungal systems have been critical to the discovery of the underlying mechanics of crossing over.

  • Several key environmental conditions that cause recombination rate variation have been identified primarily in Drosophila.

  • Recombination rate variation within a genome is in part due to ‘hotspots’ that concentrate double‐strand breaks to particular regions of the genome.

  • The demonstrated relationship between nucleotide diversity and recombination rate in Drosophila has been repeated in many organismal systems.

  • The relationship between recombination rate and genetic divergence has been less repeatable between different organismal systems, due to either mechanical or evolutionary processes.

Keywords: recombination; crossover rates; Drosophila; linkage maps; gene conversion

Figure 1.

A genetic linkage map of the four chromosomes of Drosophila. Reproduced from Morgan TH, Sturtevant AH, Muller HJ and Bridges CB (1915) The mechanism of Mendelian heredity. New York: H Holt and Company.

Figure 2.

Two major models of genetic recombination (a) Szostak DSBR model (b) Allers and Lichten SDSA model. Modified from Haber et al., . Repairing a double‐strand chromosome break by homologous recombination: revisiting Robin Holliday's model. Philosophical Transactions of the Royal Society of London Series B‐Biological Sciences359: 79–86. Reproduced with permission from The Royal Society.

close

References

Agrawal AF, Hadany L and Otto SP (2005) The evolution of plastic recombination. Genetics 171: 803–812.

Allers T and Lichten M (2001) Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106: 47–57.

Baines JF, Das A, Mousset S and Stephan W (2004) The role of natural selection in genetic differentiation of worldwide populations of Drosophila ananassae. Genetics 168: 1987–1998.

Bartolome C, Maside X and Charlesworth B (2002) On the abundance and distribution of transposable elements in the genome of Drosophila melanogaster. Molecular Biology and Evolution 19: 926–937.

Begun DJ and Aquadro CF (1992) Levels of naturally occurring DNA polymorphism correlate with recombination rates in Drosophila melanogaster. Nature 356: 519–520.

Begun DJ, Holloway AK, Stevens K et al. (2007) Population genomics: Whole‐genome analysis of polymorphism and divergence in Drosophila simulans. Plos Biology 5: 2534–2559.

Bridges CB (1927) The relation of the age of the female to crossing over in the third chromosome of Drosophila melanogaster. Journal of General Physiology 8: 689–700.

Bridges CB (1929) Variation in crossing over in relation to the age of the female in Drosophila melanogaster. Carnegie Institute of Washington Publication 399: 63–89.

Comeron JM and Kreitman M (2002) Population, evolutionary and genomic consequences of interference selection. Genetics 161: 389–410.

D'Amours D and Jackson SP (2002) The Mre11 complex: at the crossroads of DNA repair and checkpoint signalling. Nature Reviews Molecular Cell Biology 3: 317–327.

Dolgin ES and Charlesworth B (2008) The effects of recombination rate on the distribution and abundance of transposable elements. Genetics 178: 2169–2177.

Frazer KA, Ballinger DG, Cox DR et al. (2007) A second generation human haplotype map of over 3.1 million SNPs. Nature 449: 851–853.

Haber JE, Ira G, Malkova A and Sugawara N (2004) Repairing a double‐strand chromosome break by homologous recombination: revisiting Robin Holliday's model. Philosophical Transactions of the Royal Society of London Series B. Biological Sciences 359: 79–86.

Hadany L and Beker T (2003) On the evolutionary advantage of fitness‐associated recombination. Genetics 165: 2167–2179.

Hey J and Kliman RM (2002) Interactions between natural selection, recombination and gene density in the genes of Drosophila. Genetics 160: 595–608.

Hill WG and Robertson A (1966) The effect of linkage on the limits to artificial selection. Genetical Research 8: 269–294.

Hilliker AJ, Harauz G, Reaume AG et al. (1994) Meiotic gene conversion tract length distribution within the rosy locus of Drosophila melanogaster. Genetics 137: 1019–1024.

Keeney S, Giroux CN and Kleckner N (1997) Meiosis‐specific DNA double‐strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88: 375–384.

Kliman RM and Hey J (2003) Hill‐Robertson interference in Drosophila melanogaster: reply to Marais, Mouchiroud and Duret. Genetical Research 81: 89–90.

Kulathinal RJ, Bennett SM, Fitzpatrick CL and Noor MAF (2008) Fine‐scale mapping of recombination rate in Drosophila refines its correlation to diversity and divergence. Proceedings of the National Academy of Sciences of the USA 105: 10051–10056.

Lercher MJ and Hurst LD (2002) Human SNP variability and mutation rate are higher in regions of high recombination. Trends in Genetics 18: 337–340.

Marais G (2003) Biased gene conversion: implications for genome and sex evolution. Trends in Genetics 19: 330–338.

Marais G, Mouchiroud D and Duret L (2001) Does recombination improve selection on codon usage? Lessons from nematode and fly complete genomes. Proceedings of the National Academy of Sciences of the USA 98: 5688–5692.

de Massy B (2003) Distribution of meiotic recombination sites. Trends in Genetics 19: 514–522.

Myers S, Freeman C, Auton A, Donnelly P and McVean G (2008) A common sequence motif associated with recombination hot spots and genome instability in humans. Nature Genetics 40: 1124–1129.

Neel JV (1941) A relation between larval nutrition and the frequency of crossing over in the third chromosome of Drosophila melanogaster. Genetics 26: 506–516.

Noor MAF (2008) Mutagenesis from meiotic recombination is not a primary driver of sequence divergence between Saccharomyces species. Molecular Biology and Evolution 25: 2439–2444.

Noor MAF and Kliman RM (2003) Variability on the dot chromosome in the Drosophila simulans clade. Genetica 118: 51–58.

Orr‐Weaver TL, Szostak JW and Rothstein RJ (1981) Yeast transformation – a model system for the study of recombination. Proceedings of the National Academy of Sciences of the United States of America. Biological Sciences 78: 6354–6358.

Parsons PA (1988) Evolutionary rates – effects of stress upon recombination. Biological Journal of the Linnean Society 35: 49–68.

Plough HH (1917) The effect of temperature on crossing over in Drosophila. Journal of Experimental Zoology 24: 147–209.

Plough HH (1921) Further studies on the effect of temperature on crossing over. Journal of Experimental Zoology 32: 187–202.

Presgraves DC (2005) Recombination enhances protein adaptation in Drosophila melanogaster. Current Biology 15: 1651–1656.

Priest NK, Roach DA and Galloway LF (2007) Mating‐induced recombination in fruit flies. Evolution 61: 160–167.

Redfield H (1966) Delayed mating and relationship of recombination to maternal age in Drosophila melanogaster. Genetics 53: 593–607.

Spencer CCA, Deloukas P, Hunt S et al. (2006) The influence of recombination on human genetic diversity. Plos Genetics 2: 1375–1385.

Stahl FW (1994) The Holliday Junction on its 30th anniversary. Genetics 138: 241–246.

Strathern JN, Shafer BK and Mcgill CB (1995) DNA‐synthesis errors associated with double‐strand‐break repair. Genetics 140: 965–972.

Sturtevant AH (1913) The linear arrangement of six sex‐linked factors in Drosophila, as shown by their mode of association. Journal of Experimental Zoology 14: 43–59.

Symington LS (2002) Role of RAD52 epistasis group genes in homologous recombination and double‐strand break repair. Microbiology and Molecular Biology Reviews 66: 630–670.

Szostak JW, Orr‐Weaver TL, Rothstein RJ and Stahl FW (1983) The double‐strand‐break repair model for recombination. Cell 33: 25–35.

Further Reading

Nachman MW (2002) Variation in recombination rate across the genome: evidence and implications. Current Opinion in Genetics & Development 12: 657–663.

Neale MJ and Keeney S (2006) Clarifying the mechanics of DNA strand exchange in meiotic recombination. Nature 442: 153–158.

Nishant KT and Rao MRS (2006) Molecular features of meiotic recombination hot spots. Bioessays 28: 45–56.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Stevison, Laurie S, and Noor, Mohamed A F(Sep 2009) Recombination Rates in Drosophila. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021731]