Genome differentiation of Drosophila melanogaster from a microclimate contrast in Evolution Canyon, Israel

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

Volumn 110, Issue 52, 2013, Pages 21059-21064

  Hübner, Sariel ^a,b   Rashkovetsky, Eugenia ^a   Kim, Young Bun ^c   Oh, Jung Hun ^d   Michalak, Katarzyna ^c   Weiner, Dmitry ^a   Korol, Abraham B ^a   Nevo, Eviatar ^a   Michalak, Pawel ^c  

^a UNIVERSITY OF HAIFA   (Israel)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c VIRGINIA BIOINFORMATICS INSTITUTE   (United States)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Adaptive evolution; Genome sequencing; Sequence divergence

Indexed keywords

ARTICLE; DNA SEQUENCE; DROSOPHILA MELANOGASTER; EVOLUTIONARY ADAPTATION; GENE FREQUENCY; GENE ONTOLOGY; GENETIC RECOMBINATION; GENETIC VARIABILITY; GENOME; ISRAEL; LIFE HISTORY; MATING; MICROCLIMATE; NONHUMAN; PRIORITY JOURNAL; SELECTIVE SWEEP; SINGLE NUCLEOTIDE POLYMORPHISM; STRESS;

EID: 84891369622     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1321533111     Document Type: Article

References (61)

1. Korol AB, Preygel IA, Preygel SI (1994) Recombination Variability and Evolution: Algorithms of Estimation and Population-Genetic Models (Chapman & Hall, London).
2. James AC, Partridge L (1995) Thermal evolution of rate of larval development in Drosophila melanogaster in laboratory and field populations. J Evol Biol 8(3): 315-330.
3. Hoffmann AA, Harshman LG (1999) Desiccation and starvation resistance in Drosophila: Patterns of variation at the species, population and intrapopulation levels. Heredity (Edinb) 83(Pt 6): 637-643.
4. Pétavy G, Morin JP, Moreteau B, David JR (1997) Growth temperature and phenotypic plasticity in two Drosophila sibling species: Probable adaptive changes in flight capacities. J Evol Biol 10(6): 875-887.
5. Chakir M, Chafik A, Moreteau B, Gibert P, David JR (2002) Male sterility thermal thresholds in Drosophila: D. simulans appears more cold-adapted than its sibling D. melanogaster. Genetica 114(2): 195-205.
6. Hoffmann AA, Shirriffs J, Scott M (2005) Relative importance of plastic vs genetic factors in adaptive differentiation: Geographical variation for stress resistance in Drosophila melanogaster from eastern Australia. Funct Ecol 19(2): 222-227.
7. Sarup P, Sørensen JG, Dimitrov K, Barker JS, Loeschcke V (2006) Climatic adaptation of Drosophila buzzatii populations in southeast Australia. Heredity (Edinb) 96(6): 479-486.
8. Bubliy OA, Loeschcke V (2005) Variation of life-history and morphometrical traits in Drosophila buzzatii and Drosophila simulans collected along an altitudinal gradient from a Canary island. Biol J Linn Soc Lond 84(1): 119-136.
9. Hoffmann AA, Sorensen JG, Loeschcke V (2003) Adaptation of Drosophila to temperature extremes: Bringing together quantitative and molecular approaches. J Therm Biol 28(3): 175-216.
10. Kolaczkowski B, Kern AD, Holloway AK, Begun DJ (2011) Genomic differentiation between temperate and tropical Australian populations of Drosophila melanogaster. Genetics 187(1): 245-260.
11. Pavlíček T, Sharon D, Kravchenko V, Saaroni H, Nevo E (2003) Microclimatic interslope differences underlying biodiversity contrasts in "Evolution Canyon", Mt. Carmel, Israel. Isr J Earth Sci 52: 1-9.
12. Nevo E (1995) Asian, African and European biota meet at Evolution-Canyon Israel: Local tests of global biodiversity and genetic diversity patterns. Proc R Soc Lond B 262(1364): 149-155.
13. Nevo E (1997) Evolution in action across phylogeny caused by microclimatic stresses at "Evolution Canyon" Theor Popul Biol 52(3): 231-243.
14. Sikorski J, Nevo E (2005) Adaptation and incipient sympatric speciation of Bacillus simplex under microclimatic contrast at "Evolution Canyons" I and II, Israel. Proc Natl Acad Sci USA 102(44): 15924-15929.
15. Nevo E (2001) Evolution of genome-phenome diversity under environmental stress. Proc Natl Acad Sci USA 98(11): 6233-6240.
16. Nevo E (2012) "Evolution Canyon, " a potential microscale monitor of global warming across life. Proc Natl Acad Sci USA 109(8): 2960-2965.
17. 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.
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.
19. 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.
20. 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.
21. 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.
22. 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.
23. 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.
24. Zamorzaeva I, Rashkovetsky E, Nevo E, Korol A (2005) Sequence polymorphism of candidate behavioural genes in Drosophila melanogaster flies from 'Evolution canyon' Mol Ecol 14(10): 3235-3245.
25. Zamorzaeva I, Rashkovetsky E, Nevo E, Korol A (2009) Deletions in the desaturase2 gene in Israeli populations of Drosophila melanogaster: Possible role in mate recognition. Insect Mol Biol 18(1): 61-69.
26. Rashkovetsky E, et al. (2006) Adaptive differentiation of thermotolerance in Drosophila along a microclimatic gradient. Heredity (Edinb) 96(5): 353-359.
27. Iliadi KG, et al. (2009) [Peculiarities of the courtship song in the Drosophila melanogaster populations adapted to gradient of microecological conditions]. Zh Evol Biokhim Fiziol 45(5): 478-485.
28. 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.
29. Turner TL, Hahn MW, Nuzhdin SV (2005) Genomic islands of speciation in Anopheles gambiae. PLoS Biol 3(9):e285.
30. Michel AP, et al. (2010) Widespread genomic divergence during sympatric speciation. Proc Natl Acad Sci USA 107(21): 9724-9729.
31. Begun DJ, Aquadro CF (1992) Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature 356(6369): 519-520.
32. Hudson RR (1994) How can the low levels of DNA sequence variation in regions of the drosophila genome with low recombination rates be explained? Proc Natl Acad Sci USA 91(15): 6815-6818.
33. Korol AB (2013) Recombination. Encyclopedia of Biodiversity, ed Levin SA (Academic, Waltham, MA), 2nd Ed, pp 353-369.
34. Lidzbarsky GA, Shkolnik T, Nevo E (2009) Adaptive response to DNA-damaging agents in natural Saccharomyces cerevisiae populations from "Evolution Canyon", Mt. Carmel, Israel. PLoS ONE 4(6):e5914.
35. 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.
36. 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.
37. Krebs RA, Feder ME (1997) Deleterious consequences of Hsp70 overexpression in Drosophila melanogaster larvae. Cell Stress Chaperones 2(1): 60-71.
38. 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.
39. Fabian DK, et al. (2012) Genome-wide patterns of latitudinal differentiation among populations of Drosophilamelanogaster fromNorthAmerica.Mol Ecol 21(19): 4748-4769.
40. Boitard S, Schlötterer C, Nolte V, Pandey RV, Futschik A (2012) Detecting selective sweeps from pooled next-generation sequencing samples. Mol Biol Evol 29(9): 2177-2186.
41. Pool JE, et al. (2012) Population Genomics of sub-saharan Drosophila melanogaster: African diversity and non-African admixture. PLoS Genet 8(12):e1003080.
42. Hall LM, Spierer P (1986) The Ace locus of Drosophila melanogaster: Structural gene for acetylcholinesterase with an unusual 5' leader. EMBO J 5(11): 2949-2954.
43. Karasov T, Messer PW, Petrov DA (2010) Evidence that adaptation in Drosophila is not limited by mutation at single sites. PLoS Genet 6(6):e1000924.
44. Menozzi P, Shi MA, Lougarre A, Tang ZH, Fournier D (2004) Mutations of acetylcholinesterase which confer insecticide resistance in Drosophila melanogaster populations. BMC Evol Biol 4:4.
45. Sella G, Petrov DA, Przeworski M, Andolfatto P (2009) Pervasive natural selection in the Drosophila genome? PLoS Genet 5(6):e1000495.
46. Burke MK, et al. (2010) Genome-wide analysis of a long-term evolution experiment with Drosophila. Nature 467(7315): 587-590.
47. Smith JM, Haigh J (2007) The hitch-hiking effect of a favourable gene. Genet Res 89(5-6): 391-403.
48. Kaplan NL, Hudson RR, Langley CH (1989) The "hitchhiking effect" revisited. Genetics 123(4): 887-899.
49. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123(3): 585-595.
50. Fay JC, Wu CI (2000) Hitchhiking under positive Darwinian selection. Genetics 155(3): 1405-1413.
51. Kim Y, Nielsen R (2004) Linkage disequilibrium as a signature of selective sweeps. Genetics 167(3): 1513-1524.
52. Aguade M, Miyashita N, Langley CH (1989) Reduced variation in the yellow-achaetescute region in natural populations of Drosophila melanogaster. Genetics 122(3): 607-615.
53. Andolfatto P, Przeworski M (2001) Regions of lower crossing over harbor more rare variants in African populations of Drosophila melanogaster. Genetics 158(2): 657-665.
54. 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.
55. 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.
56. Kirkpatrick M, Ravigné V (2002) Speciation by natural and sexual selection: Models and experiments. Am Nat 159(Suppl 3):S22-S35.
57. McKinnon JS, et al. (2004) Evidence for ecology's role in speciation. Nature 429(6989): 294-298.
58. Schluter D (2001) Ecology and the origin of species. Trends Ecol Evol 16(7): 372-380.
59. Papadopulos AST, Baker WJ, Savolainen V (2013) Sympatric speciation in plants: The natural laboratory of Lor Howe Island. Speciation: Natural Processes, Genetics, and Biodiversity, ed Michalak P (Nova Science Publishers, New York), pp 37-57.
60. Nevo E (2011) Selection overrules gene flow at "Evolution Canyons", Israel. Advance in Genetics Research, ed Urbano KV (Nova Science Publishers, New York), pp 67-89.
61. Marais G, Mouchiroud D, Duret L (2001) Does recombination improve selection on codon usage? Lessons from nematode and fly complete genomes. Proc Natl Acad Sci USA 98(10): 5688-5692.