#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Parallel Gene Expression Differences between Low and High Latitude Populations of and .


While gene expression variation in natural populations is common, the population genetic processes responsible for the maintenance of this variation remain obscure. Here we study geographic differences in gene expression in recently established low and high latitude populations of two closely related species of Drosophila. We observe substantial parallelism in expression differences and expression plasticity between populations, which supports the idea that spatially varying selection correlated with latitude contributes to the maintenance of gene expression variation in these species. Comparison of inter-population sequence differentiation and expression differentiation suggests that cis-acting variants play a role in geographic expression differentiation.


Vyšlo v časopise: Parallel Gene Expression Differences between Low and High Latitude Populations of and .. PLoS Genet 11(5): e32767. doi:10.1371/journal.pgen.1005184
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005184

Souhrn

While gene expression variation in natural populations is common, the population genetic processes responsible for the maintenance of this variation remain obscure. Here we study geographic differences in gene expression in recently established low and high latitude populations of two closely related species of Drosophila. We observe substantial parallelism in expression differences and expression plasticity between populations, which supports the idea that spatially varying selection correlated with latitude contributes to the maintenance of gene expression variation in these species. Comparison of inter-population sequence differentiation and expression differentiation suggests that cis-acting variants play a role in geographic expression differentiation.


Zdroje

1. Futuyma D. Evolution. Third Edit. Sinauer Associates, Inc. 2013; p. 656.

2. Carson HL. Three flies and three islands: parallel evolution in Drosophila. Proc Natl Acad Sci U S A. 1974;71: 3517–3521. 4530320

3. Anderson PR, Oakeshott JG. Parallel geographical patterns of allozyme variation in two sibling Drosophila species. Nature. 1984;308: 729–731

4. Sucena E, Delon I, Jones I, Payre F, Stern DL. Regulatory evolution of shavenbaby/ovo underlies multiple cases of morphological parallelism. Nature. 2003;424: 935–938. 12931187

5. Wood TE, Burke JM, Rieseberg LH. Parallel genotypic adaptation: When evolution repeats itself. Genetica. 2005;123: 157–170. 15881688

6. Steiner CC, Weber JN, Hoekstra HE. Adaptive variation in beach mice produced by two interacting pigmentation genes. PLoS Biol. 2007;5: 1880–1889.

7. Linnen CR, Kingsley EP, Jensen JD, Hoekstra HE. On the origin and spread of an adaptive allele in deer mice. Science. 2009;325: 1095–8. doi: 10.1126/science.1175826 19713521

8. Rosenblum EB, Römpler H, Schöneberg T, Hoekstra HE. Molecular and functional basis of phenotypic convergence in white lizards at White Sands. Proc Natl Acad Sci U S A. 2010;107: 2113–2117. doi: 10.1073/pnas.0911042107 20080544

9. Grant BS, Owen DF, Clarke CA. Parallel rise and fall of melanic peppered moths in America and Britain. J Hered. 1996;87: 351–357.

10. Jeffery WR. Regressive evolution in Astyanax cavefish. Annu Rev Genet. 2009;43: 25–47. doi: 10.1146/annurev-genet-102108-134216 19640230

11. David J, Capy P. Genetic variation of Drosophila melanogaster natural populations. Trends Genet. 1988;4:106–111. 3149056

12. Singh RS, Long AD. Geographic variation in Drosophila: From molecules to morphology and back. Trends Ecol Evol. 1992;7: 340–345. doi: 10.1016/0169-5347(92)90127-W 21236059

13. Hoffmann AA, Shirriffs J, Scott M. Relative importance of plastic vs genetic factors in adaptive differentiation: Geographical variation for stress resistance in Drosophila melanogaster from eastern Australia. Funct Ecol. 2005;19: 222–227.

14. Fabian DK, Kapun M, Nolte V, Kofler R, Schmidt PS, Schlötterer C, et al. Genome-wide patterns of latitudinal differentiation among populations of Drosophila melanogaster from North America. Mol Ecol. 2012;21: 4748–4769. doi: 10.1111/j.1365-294X.2012.05731.x 22913798

15. Reinhardt JA, Kolaczkowski B, Jones CD, Begun DJ, Kern AD. Parallel geographic variation in Drosophila melanogaster. 2014;197: 361–373. doi: 10.1534/genetics.114.161463 24610860

16. Keller A. Drosophila melanogaster’s history as a human commensal. Curr Biol. 2007; 17: R77–81. 17276902

17. Stephan W, Li H. The recent demographic and adaptive history of Drosophila melanogaster. Heredity. 2007;98: 65–68. 17006533

18. Duchen P, Zivkovic D, Hutter S, Stephan W, Laurent S. Demographic inference reveals African and European admixture in the North American Drosophila melanogaster population. Genetics. 2013;193: 291–301. doi: 10.1534/genetics.112.145912 23150605

19. Dean MD, Ballard JWO. Linking phylogenetics with population genetics to reconstruct the geographic origin of a species. Mol Phylogenet Evol. 2004;32: 998–1009. 15288072

20. Aquadro CF, Lado KM, Noon WA. The rosy region of Drosophila melanogaster and Drosophila simulans. I. Contrasting levels of naturally occurring DNA restriction map variation and divergence. Genetics. 1988;119: 875–88. 2900794

21. Begun DJ, Lindfors HA, Kern AD, Jones CD. Evidence for de novo evolution of testis-expressed genes in the Drosophila yakuba/Drosophila erecta clade. Genetics. 2007;176: 1131–1137. 17435230

22. Knibb WR. Chromosome inversion polymorphisms in Drosophila melanogaster II. Geographic clines and climatic associations in Australasia, North America and Asia. Genetica. 1982;58: 213–221.

23. Turner TL, Levine MT, Eckert ML, Begun DJ. Genomic analysis of adaptive differentiation in Drosophila melanogaster. Genetics. 2008;179: 455–473. doi: 10.1534/genetics.107.083659 18493064

24. Ashburner M, Lemeunier F. Relationships within the melanogaster species subgroup of the genus Drosophila (Sophophora). I. Inversion polymorphisms in Drosophila melanogaster and Drosophila simulans. Proc R Soc B Biol Sci. 1976;193: 137–157. 5729

25. Singh RS, Choudhary M, David JR. Contrasting patterns of geographic variation in the cosmopolitan sibling species Drosophila melanogaster and Drosophila simulans. Biochem Genet. 1987;25: 27–40. 3107542

26. Singh RS. Population genetics and evolution of species related to Drosophila melanogaster. Annu Rev Genet. 1989;23: 425–53. 2515792

27. Arthur AL, Weeks AR, Sgrò CM. Investigating latitudinal clines for life history and stress resistance traits in Drosophila simulans from eastern Australia. J Evol Biol. 2008;21: 1470–1479. doi: 10.1111/j.1420-9101.2008.01617.x 18811666

28. Gibert P, Moreteau B, Pétavy G, Karan D, David JR. Chill-coma tolerance, a major climatic adaptation among Drosophila species. Evolution. 2001;55: 1063–1068. 11430643

29. Imasheva AG, Bubli OA, Lazebny OE. Variation in wing length in Eurasian natural populations of Drosophila melanogaster. Heredity. 1994;72: 508–514. 8014061

30. James AC, Azevedo RB, Partridge L. Cellular basis and developmental timing in a size cline of Drosophila melanogaster. Genetics. 1995;140: 659–666. 7498744

31. van’t Land J, van Putten P, Zwaan B, Kamping A, van Delden W. Latitudinal variation in wild populations of Drosophila melanogaster: heritabilities and reaction norms. J Evol Biol. 1999;12: 222–232.

32. Calboli FCF, Kennington WJ, Partridge L. QTL mapping reveals a striking coincidence in the positions of genomic regions associated with adaptive variation in body size in parallel clines of Drosophila melanogaster on different continents. Evolution. 2003;57: 2653. 14686541

33. Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4: 44–57. doi: 10.1038/nprot.2008.211 19131956

34. Boyle EI, Weng S, Gollub J, Jin H, Botstein D. GO::TermFinder—open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics. 2004;20: 3710–5. 15297299

35. Telonis-Scott M, Hallas R, McKechnie SW, Wee CW, Hoffmann AA. Selection for cold resistance alters gene transcript levels in Drosophila melanogaster. J Insect Physiol. 2009;55: 549–555. doi: 10.1016/j.jinsphys.2009.01.010 19232407

36. Hutter S, Saminadin-Peter SS, Stephan W, Parsch J. Gene expression variation in African and European populations of Drosophila melanogaster. Genome Biol. 2008;9: R12. doi: 10.1186/gb-2008-9-1-r12 18208589

37. Huylmans AK, Parsch J. Population- and Sex-Biased Gene Expression in the excretion organs of Drosophila melanogaster. G3 (Bethesda). 2014;4:2307–15. doi: 10.1534/g3.114.013417 25246242

38. Montell C. The TRP superfamily of cation channels. Sci STKE. 2005;2005: re3. 15728426

39. Chen Y, Lee SF, Blanc E, Reuter C, Wertheim B, Martinez-Diaz P, et al. Genome-wide transcription analysis of clinal genetic variation in Drosophila. PLoS One. 2012;7: e34620. doi: 10.1371/journal.pone.0034620 22514645

40. Yanai I, Benjamin H, Shmoish M, Chalifa-Caspi V, Shklar M, Ophir R, et al. Genome-wide midrange transcription profiles reveal expression level relationships in human tissue specification. Bioinformatics. 2005;21: 650–659. 15388519

41. Zhao L, Saelao P, Jones CD, Begun DJ. Origin and spread of de novo genes in Drosophila melanogaster populations. Science. 2014;343: 769–772. doi: 10.1126/science.1248286 24457212

42. Chintapalli VR, Wang J, Dow JA. Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat Genet. 2007;39: 715–720. 17534367

43. Parisi M, Nuttall R, Edwards P, Minor J, Naiman D, Lü J, et al. A survey of ovary-, testis-, and soma-biased gene expression in Drosophila melanogaster adults. Genome Biol. 2004;5: R40. 15186491

44. Graveley BR, Brooks AN, Carlson JW, Duff MO, Landolin JM, Yang L, et al. The developmental transcriptome of Drosophila melanogaster. Nature. 2011;471: 473–479. doi: 10.1038/nature09715 21179090

45. Meiklejohn CD, Parsch J, Ranz JM, Hartl DL. Rapid evolution of male-biased gene expression in Drosophila. Proc Natl Acad Sci U S A. 2003;100: 9894–9899. 12907700

46. Chang PL, Dunham JP, Nuzhdin S V, Arbeitman MN. Somatic sex-specific transcriptome differences in Drosophila revealed by whole transcriptome sequencing. BMC Genomics. 2011;12: 364. doi: 10.1186/1471-2164-12-364 21756339

47. Voelker RA, Cockerham CC, Johnson FM. Inversions fail to account for allozyme clines. Genetics. 1978;88:515–527. 17248810

48. Kapun M, Van Schalkwyk H, McAllister B, Flatt T, Schlötterer C. Inference of chromosomal inversion dynamics from Pool-Seq data in natural and laboratory populations of Drosophila melanogaster. Mol Ecol. 2014;23: 1813–1827. doi: 10.1111/mec.12594 24372777

49. Kolaczkowski B, Kern AD, Holloway AK, Begun DJ. Genomic differentiation between temperate and tropical Australian populations of Drosophila melanogaster. 2011;187: 245–260. doi: 10.1534/genetics.110.123059 21059887

50. Massouras A, Waszak SM, Albarca-Aguilera M, Hens K, Holcombe W, Ayroles JF, et al. Genomic variation and its impact on gene expression in Drosophila melanogaster. PLoS Genet. 2012;8: e1003055. doi: 10.1371/journal.pgen.1003055 23189034

51. Levine MT, Eckert ML, Begun DJ. Whole-genome expression plasticity across tropical and temperate Drosophila melanogaster populations from Eastern Australia. Mol Biol Evol. 2011;28: 249–56. doi: 10.1093/molbev/msq197 20671040

52. Wittkopp PJ, Haerum BK, Clark AG. Evolutionary changes in cis and trans gene regulation. Nature. 2004;430: 85–8. 15229602

53. Wittkopp PJ, Kalay G. Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat Rev Genet. 2012;13: 59–69. doi: 10.1038/nrg3095 22143240

54. Gayral P, Melo-Ferreira J, Glémin S, Bierne N, Carneiro M, Nabholz B, et al. Reference-free population genomics from next-generation transcriptome data and the vertebrate-invertebrate gap. PLoS Genet. 2013;9: e1003457. doi: 10.1371/journal.pgen.1003457 23593039

55. Wray GA. The evolutionary significance of cis-regulatory mutations. Nat Rev Genet. 2007;8: 206–216. 17304246

56. Saminadin-Peter SS, Kemkemer C, Pavlidis P, Parsch J. Selective sweep of a cis-regulatory sequence in a non-African population of Drosophila melanogaster. Mol Biol Evol. 2012;29: 1167–1174. doi: 10.1093/molbev/msr284 22101416

57. Langley CH, Stevens K, Cardeno C, Lee YCG, Schrider DR, Pool JE, et al. Genomic Variation in Natural Populations of Drosophila melanogaster. Genetics. 2012;192: 533–598. doi: 10.1534/genetics.112.142018 22673804

58. DeWitt TJ, Scheiner SM. Phenotypic plasticity: functional and conceptual approaches. New York Oxford Univ Press. 2004; 247.

59. Kuersten S, Goodwin EB. The power of the 3’ UTR: translational control and development. Nat Rev Genet. 2003;4: 626–637. 12897774

60. Merritt C, Rasoloson D, Ko D, Seydoux G. 3′ UTRs Are the primary regulators of gene expression in the C. elegans germline. Curr Biol. 2008;18: 1476–1482. doi: 10.1016/j.cub.2008.08.013 18818082

61. Mitchell-Olds T, Willis JH, Goldstein DB. Which evolutionary processes influence natural genetic variation for phenotypic traits? Nat Rev Genet. 2007;8: 845–856. 17943192

62. Gibert P, Capy P, Imasheva A, Moreteau B, Morin JP, Petavy G, et al. Comparative analysis of morphological traits among Drosophila melanogaster and D. simulans: genetic variability, clines and phenotypic plasticity. Genetica. 2004;120: 165–179. 15088656

63. Li Y, Álvarez OA, Gutteling EW, Tijsterman M, Fu J, Riksen JAG, et al. Mapping determinants of gene expression plasticity by genetical genomics in C. elegans. PLoS Genet. 2006;2: 2155–2161.

64. Grishkevich V, Yanai I. The genomic determinants of genotype X environment interactions in gene expression. Trends in Genetics. 2013;8: 479–487. doi: 10.1016/j.tig.2013.05.006 23769209

65. Spieth HT, Hsu TC. The influence of light on the matsping behavior of seven species of the Drosophila melanogaster species group. Evolution. 1950;4:316–325.

66. Barbagallo B, Garrity PA. Temperature sensation in Drosophila. Curr Opin Neurobiol. 2015;34C: 8–13. doi: 10.1016/j.conb.2015.01.002 25616212

67. Busto M, Iyengar B, Campos AR. Genetic dissection of behavior: modulation of locomotion by light in the Drosophila melanogaster larva requires genetically distinct visual system functions. J Neurosci. 1999;19: 3337–44. 10212293

68. Kaneko H, Head LM, Ling J, Tang X, Liu Y, Hardin PE, et al. Circadian rhythm of temperature preference and its neural control in Drosophila. Curr Biol. 2012;22: 1851–7. doi: 10.1016/j.cub.2012.08.006 22981774

69. Claridge-Chang A, Wijnen H, Naef F, Boothroyd C, Rajewsky N, Young MW. Circadian Regulation of Gene Expression Systems in the Drosophila Head. Neuron. 2001;32: 657–671. 11719206

70. Aho AC, Donner K, Hydén C, Larsen LO, Reuter T. Low retinal noise in animals with low body temperature allows high visual sensitivity. Nature. 1988;334: 348–50. 3134619

71. Juusola M, Hardie RC. Light adaptation in Drosophila photoreceptors: II. Rising temperature increases the bandwidth of reliable signaling. J Gen Physiol. 2001;117: 27–42. 11134229

72. Rogers RL, Cridland JM, Shao L, Hu TT, Andolfatto P, Thornton KR. Landscape of standing variation for tandem duplications in Drosophila yakuba and Drosophila simulans. Mol Biol Evol. 2014;31: 1750–1766. doi: 10.1093/molbev/msu124 24710518

73. David JR, Allemand R, Capy P, Chakir M, Gibert P, Pétavy G, et al. Comparative life histories and ecophysiology of Drosophila melanogaster and D. simulans. Genetica. 2004;120: 151–163. 15088655

74. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009;25: 1105–1111. doi: 10.1093/bioinformatics/btp120 19289445

75. Hu TT, Eisen MB, Thornton KR, Andolfatto P. A second generation assembly of the Drosophila simulans genome provides new insights into patterns of lineage-specific divergence. Genome Res. 2013;23: 89–98. doi: 10.1101/gr.141689.112 22936249

76. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-Seq data with DESeq2. Genome Biol. 2014;15:550. 25516281

77. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26: 139–140. doi: 10.1093/bioinformatics/btp616 19910308

78. Smyth GK, Ritchie M, Thorne N. Linear Models for Microarray Data User’ s Guide. Bioinformatics. 2011;20: 3705–3706.

79. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B. 1995;57: 289–300.

80. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010;28: 516–520. doi: 10.1038/nbt.1626 20436463

81. Tang H, Wang XX, Bowers JE, Ming R, Alam M, Paterson AH, et al. Unraveling ancient hexaploidy through multiply-aligned angiosperm gene maps. Genome Res. 2008;18: 1944–1954. doi: 10.1101/gr.080978.108 18832442

82. Corbett-Detig RB, Hartl DL. Population genomics of inversion polymorphisms in Drosophila melanogaster. PLoS Genet. 2012;8: e1003056. doi: 10.1371/journal.pgen.1003056 23284285

83. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25: 1754–1760. doi: 10.1093/bioinformatics/btp324 19451168

84. Kofler R, Pandey RV, Schlötterer C. PoPoolation2: Identifying differentiation between populations using sequencing of pooled DNA samples (Pool-Seq). Bioinformatics. 2011;27: 3435–3436. doi: 10.1093/bioinformatics/btr589 22025480

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2015 Číslo 5
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#