Divergence of Drosophila melanogaster repeatomes in response to a sharp microclimate contrast in Evolution Canyon, Israel

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 29, 2014, Pages 10630-10635

  Kim, Young Bun ^a   Oh, Jung Hun ^c   McIver, Lauren J ^a   Rashkovetsky, Eugenia ^d   Michalak, Katarzyna ^a   Garner, Harold R ^a,b   Kang, Lin ^a   Nevo, Eviatar ^d   Korol, Abraham B ^d   Michalak, Pawel ^a,b  

^a VIRGINIA BIOINFORMATICS INSTITUTE   (United States)

^b VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d UNIVERSITY OF HAIFA   (Israel)

Author keywords

Adaptive evolution; Genome sequencing; Incipient speciation; Microsatellite

Indexed keywords

DNA;

ARTICLE; ASSORTATIVE MATING; BIOTA; CLIMATE CHANGE; COGNITION; DNA STRUCTURE; DNA TRANSPOSITION; DROSOPHILA MELANOGASTER; EVOLUTIONARY RATE; FEMALE; GENE DISRUPTION; GENE SEQUENCE; GENETIC VARIABILITY; HEAT TOLERANCE; INSECT GENOME; ISRAEL; MICROCLIMATE; MOLECULAR EVOLUTION; NONHUMAN; PHENOTYPIC VARIATION; POPULATION DIFFERENTIATION; PRIORITY JOURNAL; REPEATOME; SMELLING; TRANSPOSON;

ADAPTIVE EVOLUTION; GENOME SEQUENCING; INCIPIENT SPECIATION; MICROSATELLITE;

ANIMALS; BASE SEQUENCE; BIOLOGICAL EVOLUTION; CHROMOSOMES, INSECT; DNA TRANSPOSABLE ELEMENTS; DROSOPHILA MELANOGASTER; GENETIC VARIATION; ISRAEL; MICROCLIMATE; MICROSATELLITE REPEATS; POLYMORPHISM, SINGLE NUCLEOTIDE; REPETITIVE SEQUENCES, NUCLEIC ACID; X CHROMOSOME;

EID: 84904604550     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1410372111     Document Type: Article

References (58)

1. Wang T, et al. (2007) Species-specific endogenous retroviruses shape the transcriptional network of the human tumor suppressor protein p53. Proc Natl Acad Sci USA 104(47):18613-18618. (Pubitemid 350210745)
2. Ashburner M, Golic KG, Hawley RS (2005) Drosophila: A Laboratory Handbook (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY), 2nd Ed, p xxviii.
3. Aminetzach YT, Macpherson JM, Petrov DA (2005) Pesticide resistance via trans-position-mediated adaptive gene truncation in Drosophila. Science 309(5735):764-767. (Pubitemid 41077321)
4. Sinzelle L, Izsvák Z, Ivics Z (2009) Molecular domestication of transposable elements: From detrimental parasites to useful host genes. Cell Mol Life Sci 66(6):1073-1093.
5. Joly-Lopez Z, Forczek E, Hoen DR, Juretic N, Bureau TE (2012) A gene family derived from transposable elements during early angiosperm evolution has reproductive fitness benefits in Arabidopsis thaliana. PLoS Genet 8(9):e1002931.
6. Feschotte C (2008) Transposable elements and the evolution of regulatory networks. Nat Rev Genet 9(5):397-405.
7. Iglesias AR, Kindlund E, Tammi M, Wadelius C (2004) Some microsatellites may act as novel polymorphic cis-regulatory elements through transcription factor binding. Gene 341:149-165.
8. Sirand-Pugnet P, Durosay P, Brody E, Marie J (1995) An intronic (A/U)GGG repeat enhances the splicing of an alternative intron of the chicken beta-tropomyosin premRNA. Nucleic Acids Res 23(17):3501-3507.
9. Li YC, Korol AB, Fahima T, Nevo E (2004) Microsatellites within genes: Structure, function, and evolution. Mol Biol Evol 21(6):991-1007. (Pubitemid 38658207)
10. Capy P, Gasperi G, Biémont C, Bazin C (2000) Stress and transposable elements: Coevolution or useful parasites? Heredity (Edinb) 85(Pt 2):101-106.
11. González J, Karasov TL, Messer PW, Petrov DA (2010) Genome-wide patterns of adaptation to temperate environments associated with transposable elements in Drosophila. PLoS Genet 6(4):e1000905.
12. Michalak P, et al. (2001) Genetic evidence for adaptation-driven incipient speciation of Drosophila melanogaster along a microclimatic contrast in "Evolution Canyon," Israel. Proc Natl Acad Sci USA 98(23):13195-13200. (Pubitemid 33051339)
13. Lerman DN, Michalak P, Helin AB, Bettencourt BR, Feder ME (2003) Modification of heat-shock gene expression in Drosophila melanogaster populations via transposable elements. Mol Biol Evol 20(1):135-144. (Pubitemid 36077908)
14. Krebs RA, Feder ME (1997) Deleterious consequences of Hsp70 overexpression in Drosophila melanogaster larvae. Cell Stress Chaperones 2(1):60-71. (Pubitemid 27170407)
15. Zatsepina OG, et al. (2001) A Drosophila melanogaster strain from sub-equatorial Africa has exceptional thermotolerance but decreased Hsp70 expression. J Exp Biol 204(Pt 11):1869-1881. (Pubitemid 34869505)
16. Nevo E (1995) Asian, African and European biota meet at Evolution-Canyon Israel: Local tests of global biodiversity and genetic diversity patterns. Proc Roy Soc Lond B Bio 262(1364):149-155.
17. Nevo E (2012) "Evolution Canyon," a potential microscale monitor of global warming across life. Proc Natl Acad Sci USA 109(8):2960-2965.
18. Nevo E, Rashkovetsky E, Pavlicek T, Korol A (1998) A complex adaptive syndrome in Drosophila caused by microclimatic contrasts. Heredity (Edinb) 80(Pt 1):9-16. (Pubitemid 28110980)
19. Lupu A, Pechkovskaya A, Rashkovetsky E, Nevo E, Korol A (2004) DNA repair efficiency and thermotolerance in Drosophila melanogaster from "Evolution Canyon". Mutagenesis 19(5):383-390. (Pubitemid 39405975)
20. Rashkovetsky E, et al. (2006) Adaptive differentiation of thermotolerance in Drosophila along a microclimatic gradient. Heredity (Edinb) 96(5):353-359. (Pubitemid 43670398)
21. Korol A, Rashkovetsky E, Iliadi K, Nevo E (2006) Drosophila flies in "Evolution Canyon" as a model for incipient sympatric speciation. Proc Natl Acad Sci USA 103(48):18184-18189. (Pubitemid 44871633)
22. Iliadi KG, et al. (2009) Peculiarities of the courtship song in the Drosophila melanogaster populations adapted to gradient of microecological conditions. J Evol Biochem Physiol 45(5):579-589.
23. Iliadi K, et al. (2001) Sexual and reproductive behaviour of Drosophila melanogaster from a microclimatically interslope differentiated population of "Evolution Canyon" (Mount Carmel, Israel). Proc Biol Sci 268(1483):2365-2374. (Pubitemid 33096102)
24. Korol A, et al. (2000) Nonrandom mating in Drosophila melanogaster laboratory populations derived from closely adjacent ecologically contrasting slopes at "Evolution Canyon". Proc Natl Acad Sci USA 97(23):12637-12642.
25. Debat V, et al. (2008) Multidimensional analysis of Drosophila wing variation in Evolution Canyon. J Genet 87(4):407-419.
26. Pavlicek T, Frenkel Z, Korol AB, Beiles A, Nevo E (2008) Drosophila at the "Evolution Canyon" microsite, Mt. Carmel, Israel: Selection overrules migration. Isr J Ecol Evol 54(2):165-180.
27. Hübner S, et al. (2013) Genome differentiation of Drosophila melanogaster from a microclimate contrast in Evolution Canyon, Israel. Proc Natl Acad Sci USA 110(52):21059-21064.
28. Clark AG, et al.; Drosophila 12 Genomes Consortium (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450(7167):203-218.
29. Kofler R, Betancourt AJ, Schlötterer C (2012) Sequencing of pooled DNA samples (Pool-Seq) uncovers complex dynamics of transposable element insertions in Drosophila melanogaster. PLoS Genet 8(1):e1002487.
30. Bartolomé C, Maside X, Charlesworth B (2002) On the abundance and distribution of transposable elements in the genome of Drosophila melanogaster. Mol Biol Evol 19(6):926-937. (Pubitemid 34602962)
31. Bucheton A, et al. (1992) I elements and the Drosophila genome. Genetica 86(1-3):175-190.
32. Orsi GA, Joyce EF, Couble P, McKim KS, Loppin B (2010) Drosophila I-R hybrid dysgenesis is associated with catastrophic meiosis and abnormal zygote formation. J Cell Sci 123(Pt 20):3515-3524.
33. Carmel J, Rashkovetsky E, Nevo E, Korol A (2011) Differential expression of small heat shock protein genes Hsp23 and Hsp40, and heat shock gene Hsr-omega in fruit flies (Drosophila melanogaster) along a microclimatic gradient. J Hered 102(5):593-603.
34. Singh SR, Rashkovetsky E, Iliadi K, Nevo E, Korol A (2005) Assortative mating in Drosophila adapted to a microsite ecological gradient. Behav Genet 35(6):753-764. (Pubitemid 41643186)
35. Panhuis TM, Swanson WJ, Nunney L (2003) Population genetics of accessory gland proteins and sexual behavior in Drosophila melanogaster populations from Evolution Canyon. Evolution 57(12):2785-2791. (Pubitemid 38078359)
36. Liao GC, Rehm EJ, Rubin GM (2000) Insertion site preferences of the P transposable element in Drosophila melanogaster. Proc Natl Acad Sci USA 97(7):3347-3351. (Pubitemid 30183305)
37. Walser JC, Chen B, Feder ME (2006) Heat-shock promoters: Targets for evolution by P transposable elements in Drosophila. PLoS Genet 2(10):e165.
38. Haney RA, Feder ME (2009) Contrasting patterns of transposable element insertions in Drosophila heat-shock promoters. PLoS ONE 4(12):e8486.
39. Shen Y, Lansky E, Traber M, Nevo E (2013) Increases in both acute and chronic temperature potentiate tocotrienol concentrations in wild barley at 'Evolution Canyon'. Chem Biodivers 10(9):1696-1705.
40. Harry M, et al. (1999) Fine-scale biodiversity of Drosophilidae in "Evolution Canyon" at the Lower Nahal Oren microsite, Israel. Biologia 54(6):685-705. (Pubitemid 129634976)
41. Burke MK, et al. (2010) Genome-wide analysis of a long-term evolution experiment with Drosophila. Nature 467(7315):587-590.
42. Hochman B (1976) The fourth chromosome of Drosophila melanogaster. The Genetics and Biology of Drosophila, eds Ashburner M, Novitski E (Academic Press, New York), Vol 1b, pp 903-928.
43. Rizzon C, Marais G, Gouy M, Biémont C (2002) Recombination rate and the distribution of transposable elements in the Drosophila melanogaster genome. Genome Res 12(3):400-407. (Pubitemid 34233014)
44. Duret L, Marais G, Biémont C (2000) Transposons but not retrotransposons are located preferentially in regions of high recombination rate in Caenorhabditis elegans. Genetics 156(4):1661-1669. (Pubitemid 32001233)
45. Tautz D, Schlötterer (1994) Simple sequences. Curr Opin Genet Dev 4(6):832-837.
46. Fondon JW, 3rd, Garner HR (2004) Molecular origins of rapid and continuous morphological evolution. Proc Natl Acad Sci USA 101(52):18058-18063.
47. Fondon JW, 3rd, Hammock EA, Hannan AJ, King DG (2008) Simple sequence repeats: Genetic modulators of brain function and behavior. Trends Neurosci 31(7):328-334.
48. Schlötterer C, Agis M (2002) Microsatellite analysis of Drosophila melanogaster populations along a microclimatic contrast at lower Nahel Oren canyon, Mount Carmel, Israel. Mol Biol Evol 19(4):563-568. (Pubitemid 34289432)
49. Kalendar R, Tanskanen J, Immonen S, Nevo E, Schulman AH (2000) Genome evolution of wild barley (Hordeum spontaneum) by BARE-1 retrotransposon dynamics in response to sharp microclimatic divergence. Proc Natl Acad Sci USA 97(12):6603-6607. (Pubitemid 30412760)
50. Bedada G, Westerbergh A, Nevo E, Korol A, Schmid KJ (2014) DNA sequence variation of wild barley Hordeum spontaneum (L.) across environmental gradients in Israel. Heredity (Edinb) 112(6):646-655.
51. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25(14):1754-1760.
52. Kofler R, et al. (2011) PoPoolation: A toolbox for population genetic analysis of next generation sequencing data from pooled individuals. PLoS ONE 6(1):e15925.
53. Huang W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4(1):44-57.
54. Kofler R, Pandey RV, Schlötterer C (2011) PoPoolation2: Identifying differentiation between populations using sequencing of pooled DNA samples (Pool-Seq). Bioinformatics 27(24):3435-3436.
55. McIver LJ, Fondon JW, 3rd, Skinner MA, Garner HR (2011) Evaluation of microsatellite variation in the 1000 Genomes Project pilot studies is indicative of the quality and utility of the raw data and alignments. Genomics 97(4):193-199.
56. McIver LJ, McCormick JF, Martin A, Fondon JW, 3rd, Garner HR (2013) Populationscale analysis of human microsatellites reveals novel sources of exonic variation. Gene 516(2):328-334.
57. Benson G (1999) Tandem repeats finder: A program to analyze DNA sequences. Nucleic Acids Res 27(2):573-580.
58. Karolchik D, et al. (2014) The UCSC Genome Browser database: 2014 update. Nucleic Acids Res 42(Database issue):D764-D770.