Genomic Evidence for Adaptive Inversion Clines in Drosophila melanogaster

Molecular Biology and Evolution

Volumn 33, Issue 5, 2016, Pages 1317-1336

  Kapun, Martin ^a   Fabian, Daniel K ^b   Goudet, Jérôme ^a   Flatt, Thomas ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

chromosomal inversion polymorphisms; clinal adaptation; clines; Drosophila; population genomics; spatially and temporally varying selection

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CHROMOSOME INVERSION; CHROMOSOME POLYMORPHISM; CLIMATE CHANGE; CONTROLLED STUDY; CYTOLOGY; DROSOPHILA MELANOGASTER; ENVIRONMENTAL IMPACT; EVIDENCE BASED PRACTICE; FREQUENCY ANALYSIS; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENE SEQUENCE; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GENOME ANALYSIS; GENOME-WIDE ASSOCIATION STUDY; KARYOTYPING; MALE; NONHUMAN; POPULATION; POPULATION STRUCTURE; SEASONAL VARIATION; SINGLE NUCLEOTIDE POLYMORPHISM; SPATIOTEMPORAL ANALYSIS; SUMMER; ADAPTATION; ANIMAL; EVOLUTION; GENETICS; MOLECULAR EVOLUTION; NORTH AMERICA; POPULATION GENETICS; PROCEDURES;

ADAPTATION, BIOLOGICAL; ANIMALS; BIOLOGICAL EVOLUTION; CHROMOSOME INVERSION; DROSOPHILA MELANOGASTER; EVOLUTION, MOLECULAR; GENETICS, POPULATION; LINKAGE DISEQUILIBRIUM; MALE; NORTH AMERICA; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 84966806732     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msw016     Document Type: Article

References (142)

1. Adrion JR, Hahn MW, Cooper BS. 2015. Revisiting classic clines in Drosophila melanogaster in the age of genomics. Trends Genet. 8:434-444
2. Anderson AR, Hoffmann AA, McKechnie SW, Umina PA, Weeks AR. 2005. The latitudinal cline in the In(3R)Payne inversion polymorphism has shifted in the last 20 years in Australian Drosophila melanogaster populations. Mol Ecol. 14:851-858
3. Anderson PR, Knibb WR, Oakeshott JG. 1987. Observations on the extent and temporal stability of latitudinal clines for alcohol dehydrogenase allozymes and four chromosome inversions in Drosophila melanogaster. Genetica 75:81-88
4. Anderson WW, Arnold J, Baldwin DG, Beckenbach AT, Brown CJ, Bryant SH, Coyne JA, Harshman LG, Heed WB, Jeffery DE, et al. 1991. Four decades of inversion polymorphism in Drosophila pseudoobscura. Proc Natl Acad Sci U S A. 88:10367-10371
5. Andolfatto P, Depaulis F, Navarro A. 2001. Inversion polymorphisms and nucleotide variability in Drosophila. Genet Res. 77:1-8
6. Aulard S, David JR, Lemeunier F. 2002. Chromosomal inversion polymorphism in Afrotropical populations of Drosophila melanogaster. Genet Res. 79:49-63
7. Ayala D, Fontaine MC, Cohuet A, Fontenille D, Vitalis R, Simard F. 2011. Chromosomal inversions, natural selection and adaptation in the malaria vector Anopheles funestus. Mol Biol Evol. 28:745-758
8. Balanya J, Huey RB, Gilchrist GW, Serra L. 2009. The chromosomal polymorphism of Drosophila subobscura: a microevolutionary weapon to monitor global change. Heredity 103:364-367
9. Balanya J, Oller JM, Huey RB, Gilchrist GW, Serra L. 2006. Global genetic change tracks global climate warming in Drosophila subobscura. Science 313:1773-1775
10. Bastide H, Betancourt A, Nolte V, Tobler R, Stobe P, Futschik A, Schotterer C. 2013. A genome-wide, fine-scale map of natural pigmentation variation in Drosophila melanogaster. PLoS Genet. 9:e1003534
11. Behrman EL, Watson SS, O'Brien KR, Heschel MS, Schmidt PS. 2015. Seasonal variation in life history traits in two Drosophila species. J Evol Biol. 28:1691-1704
12. Bergland AO, Behrman EL, O'Brien KR, Schmidt PS, Petrov DA. 2014. Genomic evidence of rapid and stable adaptive oscillations over seasonal time scales in Drosophila. PLoS Genet. 10:e1004775
13. Bergland AO, Tobler R, González J, Schmidt P, Petrov D. 2016. Secondary contact and local adaptation contribute to genome-wide patterns of clinal variation in Drosophila melanogaster. Mol Ecol. Advance Access publication January 18, 2016; doi: 10.1111/mec.13455
14. Bradshaw WE, Holzapfel CM. 2006. Climate change. Evolutionary response to rapid climate change. Science 312:1477-1478
15. Calboli FCF, Kennington WJ, Partridge L. 2003. 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 57:2653-2658
16. Caracristi G, Schlotterer C. 2003. Genetic differentiation between American and European Drosophila melanogaster populations could be attributed to admixture of African alleles.Mol Biol Evol. 20:792-799
17. Cheng C, White BJ, Kamdem C, Mockaitis K, Constantini C, Hahn MW, Besansky NJ. 2012. Ecological genomics of Anopheles gambiae along a latitudinal cline: a population-resequencing approach. Genetics 190:1417-1432
18. Clemente F, Vogl C. 2012. Unconstrained evolution in short introns?-an analysis of genome-wide polymorphism and divergence data from Drosophila. J Evol Biol. 25:1975-1990
19. Cogni R, Kuczynski C, Koury S, Lavington E, Behrman EL, O'Brien KR, Schmidt PS, EanesWF. 2013. The intensity of selection acting on the couch potato gene-spatial-temporal variation in a diapause cline. Evolution 68:538-548
20. Cogni R, Kuczynski K, Lavington E, Koury S, Behrman EL, O'Brien KR, Schmidt PS, Eanes WF. 2015. Variation in Drosophila melanogaster central metabolic genes appears driven by natural selection both within and between populations. Proc R Soc B Biol Sci. 282:20142688
21. Cohen J. 1988. Statistical power analysis for the behavioral sciences. 2nd ed. Hillsdale (NJ): Lawrence Earlbaum
22. Corbett-Detig RB, Hartl DL. 2012. Population genomics of inversion polymorphisms in Drosophila melanogaster. PLoS Genet. 8:e1003056
23. Coyne JA, Beecham E. 1987. Heritability of two morphological characters within and among natural populations of Drosophila melanogaster. Genetics 117:727-737
24. David JR, Bocquet C. 1975. Evolution in a cosmopolitan species: genetic latitudinal clines in Drosophila melanogaster wild populations. Experientia 31:164-166
25. David JR, Capy P. 1988. Genetic variation of Drosophila melanogaster natural populations. Trends Genet. 4:106-111
26. De Jong G, Bochdanovits Z. 2003. Latitudinal clines in Drosophila melanogaster: body size, allozyme frequencies, inversion frequencies, and the insulin-signalling pathway. J Genet. 82:207-223
27. Dobzhansky T. 1937. Genetics and the origin of species. 1st ed. New York: Columbia University Press
28. Dobzhansky T. 1943. Genetics of natural populations. IX. Temporal changes in the composition of populations of Drosophila pseudoobscura. Genetics 28:162-186
29. Dobzhansky T. 1947a. Adaptive changes induced by natural selection in wild populations of Drosophila. Evolution 1:1-16
30. Dobzhansky T. 1947b. Genetics of natural populations. XIV. A response of certain gene arrangements in the third chromosome of Drosophila pseudoobscura to Natural Selection. Genetics 32:142-160
31. Dobzhansky T. 1948. Genetics of natural populations. XVIII. Experiments on chromosomes of Drosophila pseudoobscura from different geographic regions. Genetics 33:588-602
32. Dobzhansky T. 1950. Genetics of natural populations. XIX. Origin of heterosis through natural selection in populations of Drosophila pseudoobscura. Genetics 35:288-302
33. Dobzhansky T. 1970. Genetics of the evolutionary process. New York: Columbia University Press
34. Dobzhansky T, Ayala FJ. 1973. Temporal frequency changes of enzyme and chromosomal polymorphisms in natural populations of Drosophila. Proc Natl Acad Sci U S A. 70:680-683
35. Dobzhansky T, Epling C. 1944. Taxonomy, geographic distribution, and ecology of Drosophila pseudoobscura and its relatives. Carnegie Inst Washington Pub 554:1-46
36. Duchen P, Zivkovic D, Hutter S, Stephan W, Laurent S. 2013. Demographic inference reveals African and European admixture in the North American Drosophila melanogaster population. Genetics 193:291-301
37. Endler JA. 1977. Geographic variation, speciation, and clines. Princeton (NJ): Princeton University Press
38. Endler JA. 1986. Natural selection in the wild. Princeton (NJ): Princeton University Press
39. Fabian DK, Kapun M, Nolte V, Kofler R, Schmidt PS, Schlotterer C, Flatt T. 2012. Genome-wide patterns of latitudinal differentiation among populations of Drosophila melanogaster from North America. Mol Ecol. 21:4748-4769
40. Fabian DK, Lack JB, Mathur V, Schlotterer C, Schmidt PS, Pool JE, Flatt T. 2015. Spatially varying selection shapes life history clines among populations of Drosophila melanogaster from sub-Saharan Africa. J Evol Biol. 28:826-840
41. Faria R, Neto S, Noor MAF, Navarro A. 2011. Role of natural selection in chromosomal speciation. ELS. Chichester (UK): John Wiley &Sons
42. Flatt T, Amdam GV, Kirkwood TBL, Omholt SW. 2013. Life-history evolution and the polyphenic regulation of somatic maintenance and survival. Q Rev Biol. 88:185-218
43. Flatt T, Heyland A. 2011.Mechanisms of life history evolution. In: The genetics and physiology of life history traits and trade-offs. Oxford: Oxford University Press
44. Flatt T, Schmidt PS. 2009. Integrating evolutionary and molecular genetics of aging. Biochim Biophys Acta 1790:951-962
45. Frichot E, Schoville SD, Bouchard G, Francois O. 2013. Testing for associations between loci and environmental gradients using latent factor mixed models. Mol Biol Evol. 30:1687-1699
46. Garcia-Vázquez E, Sánchez-Refusta F. 1988. Chromosomal polymorphism and extra bristles of Drosophila melanogaster: joint variation under selection in isofemale lines. Genetica 78:91-96
47. Gockel J, Robinson SJW, KenningtonWJ, Goldstein DB, Partridge L. 2002. Quantitative genetic analysis of natural variation in body size in Drosophila melanogaster. Heredity 89:145-153
48. Guerrero RF, Rousset F, Kirkpatrick M. 2012. Coalescent patterns for chromosomal inversions in divergent populations. Philos Trans R Soc Lond B Biol Sci. 367:430-438
49. Halekoh U, Højsgaard S, Yan J. 2007. The R package geepack for generalized estimating equations. J Stat Softw. 15:1-11
50. Hasson E, Eanes WF. 1996. Contrasting histories of three gene regions associated with In(3L)Payne of Drosophila melanogaster. Genetics 144:1565-1575
51. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. 2005. Very high resolution interpolated climate surfaces for global land areas. Int J Climatol. 25:1965-1978
52. Hijmans RJ, van Etten J. 2012. raster: Geographic analysis and modeling with raster data. 2012; R package version 2.0-12. [cited 2015 December 21] Available from: http://CRAN.R-project.org/ packageandfrac14;raster
53. Hoffmann AA, Rieseberg LH. 2008. Revisiting the impact of inversions in evolution: from population genetic markers to drivers of adaptive shifts and speciation? Annu Rev Ecol Evol Syst. 39:21-42
54. Hoffmann AA, Weeks AR. 2007. Climatic selection on genes and traits after a 100 year-old invasion: a critical look at the temperate-tropical clines in Drosophila melanogaster from eastern Australia. Genetica 129:133-147
55. Hoffmann AA, Sgro CM, Weeks AR. 2004. Chromosomal inversion polymorphisms and adaptation. Trends Ecol Evol. 19:482-488
56. Hoffmann AA, Sorensen JG, Loeschcke V. 2003. Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches. J Therm Biol. 28:175-216
57. Huang W, Massouras A, Inoue Y, Peiffer J, Ramia M, Tarone AM, Turlapati L, Zichner T, Zhu D, Lyman RF, et al. 2014. Natural variation in genome architecture among 205 Drosophila melanogaster Genetic Reference Panel lines. Genome Res. 24:1193-1208
58. Huey RB, Rosenzweig F. 2009. Laboratory evolution meets catch-22: balancing simplicity and realism. In: T Garland, MR Rose, editors. Experimental evolution. Berkeley (CA): University of California Press. p. 670-701
59. Inoue Y. 1979a. The fate of polymorphic inversions of Drosophila melanogaster transferred to laboratory conditions. Jap J Genet. 54:83-96
60. Inoue Y. 1979b. Seasonal changes of inversion frequencies of Drosophila melanogaster. Ann Rep Natl Inst Genet (Japan) 29:77
61. Inoue Y, Watanabe T, Watanabe TK. 1984. Evolutionary change of the chromosomal polymorphism in Drosophila melanogaster populations. Evolution 38:753-765
62. James AC, Azevedo RBR, Partridge L. 1995. Cellular basis and developmental timing in a size cline of Drosophila melanogaster. Genetics 140:659-666
63. James AC, Partridge L. 1995. Thermal evolution of rate of larval development in Drosophila melanogaster in laboratory and field populations. J Evol Biol. 8:315-330
64. JoronM, Frezal L, Jones RT, Chamberlain NL, Lee SF, Haag CR, Whibley A, Becuwe M, Baxter SW, Ferguson L, et al. 2011. Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry. Nature 477:203-206
65. Kao JY, Zubair A, SalomonMP, Nuzhdin SV, Campo D. 2015. Population genomic analysis uncovers African and European admixture in Drosophila melanogaster populations from the south-eastern United States and Caribbean Islands. Mol Ecol. 24:1499-1509
66. Kapun M, van Schalkwyk H, McAllister B, Flatt T, Schlotterer C. 2014. Inference of chromosomal inversion dynamics fromPool-Seq data in natural and laboratory populations of Drosophila melanogaster. Mol Ecol 23:1813-1827
67. Kellermann V, Hoffmann AA, Kristensen TN,MoghadamNN, Loeschcke V. 2015. Experimental evolution under fluctuating thermal conditions does not reproduce patterns of adaptive clinal differentiation in Drosophila melanogaster. Am Nat. 186:582-593
68. KenningtonWJ, Hoffmann AA. 2013. Patterns of genetic variation across inversions: geographic variation in the In(2L)t inversion in populations of Drosophila melanogaster from eastern Australia. BMC Evol Biol. 13:100
69. Kennington WJ, Hoffmann AA, Partridge L. 2007. Mapping regions within cosmopolitan inversion In(3R)Payne associated with natural variation in body size in Drosophila melanogaster. Genetics 177:549-556
70. KirkpatrickM. 2010. How and why chromosome inversions evolve. PLoS Biol 8:e1000501
71. KirkpatrickM, BartonN. 2006. Chromosome inversions, local adaptation and speciation. Genetics 173:419-434
72. Kirkpatrick M, Kern A. 2012.Where's themoney? Inversions, genes, and the hunt for genomic targets of selection. Genetics 190:1153-1155
73. Klepsatel P, Gáliková M, Huber CD, Flatt T. 2014. Similarities and differences in altitudinal versus latitudinal variation for morphological traits in Drosophila melanogaster. Evolution 68:1385-1398
74. Knibb WR. 1982. Chromosome inversion polymorphisms in Drosophila melanogaster II. Geographic clines and climatic associations in Australasia, North America and Asia. Genetica 58:213-221
75. Knibb WR. 1986. Temporal variation of Drosophila melanogaster Adh allele frequencies, inversion freqencies, and population sizes. Genetica 71:175-190
76. KnibbWR, Oakeshott JG, Gibson JB. 1981. Chromosome inversion polymorphisms in Drosophila melanogaster. I. Latitudinal clines and associations between inversions in Australasian populations. Genetics 98:833-847
77. Kofler R, Orozco-Wengel P, De Maio N, Pandey RV, Nolte V, Futschik A, Kosiol C, Schlotterer C. 2011. PoPoolation: a toolbox for population genetic analysis of next generation sequencing data from pooled individuals. PLoS One 6:e15925
78. Kolaczkowski B, Kern AD, Holloway AK, Begun DJ. 2011. Genomic differentiation between temperate and tropical Australian populations of Drosophila melanogaster. Genetics 187:245-260
79. Krimbas C. 1992. The inversion polymorphism of Drosophila subobscura. In: CB Krimbas, JR Powell, editors. Drosophila inversion polymorphism. Boca Raton (FL): CRC Press. p. 127-220
80. Krimbas CB, Powell JR. 1992. Drosophila inversion polymorphism. Boca Raton (FL): CRC Press
81. Lack JB, CardenoCM, CrepeauMW, TaylorW,Corbett-DetigRB, Stevens KA, Langley CH, Pool JE. 2015. The Drosophila genome nexus: a population genomic resource of 623 Drosophila melanogaster genomes, including 197 from a single ancestral range population. Genetics 199:1229-1241
82. Langley CH, Ito K, Voelker RA. 1977. Linkage disequilibrium in natural populations of Drosophila melanogaster. Seasonal variation. Genetics 86:447-454
83. Langley CH, Stevens K, Cardeno C, Lee YCG, Schrider DR, Pool JE, Langley SA, Suarez C, Corbett-Detig RB, Kolaczkowski B, et al. 2012. Genomic variation in natural populations of Drosophila melanogaster. Genetics 192:533-598
84. Le S, Josse J, Husson F. 2008. FactoMineR: an R package for multivariate analysis. J Stat Softw 25:1-18
85. Lemeunier F, Aulard S. 1992. Inversion polymorphism in Drosophila melanogaster. In:CBKrimbas, JRPowell, editors. Drosophila inversion polymorphism. Boca Raton (FL): CRC Press. p. 339-405
86. Levitan M. 2003. Climatic factors and increased frequencies of "southern" chromosome forms in natural populations of Drosophila robusta. Evol Ecol Res. 5:597-604
87. Levy RC, Kozak GM, Wadsworth CB, Coates BS, Dopman EB. 2015. Explaining the sawtooth: latitudinal periodicity in a circadian gene correlates with shifts in generation number. J Evol Biol. 28:40-53
88. Lewontin RC. 1974. The genetic basis of evolutionary change. New York: Columbia University Press
89. Li H. 2013. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Unpublished data, preprint. arXiv:1303.3997v2. Accessed 21 December 2015
90. Lowry DB, Willis JH. 2010. A widespread chromosomal inversion polymorphism contributes to a major life-history transition, local adaptation, and reproductive isolation. PLoS Biol. 8:e1000500
91. Mackay TFC, Richards S, Stone EA, Barbadilla A, Ayroles JF, Zhu D, Casillas S, Han Y, Magwire MM, Cridland JM, et al. 2012. The Drosophila melanogaster genetic reference panel. Nature 482:173-178
92. Masry AM. 1981. The evolutionary changes of the population structure. I. Seasonal changes in the frequencies of chromosomal inversions in natural populations of D. melanogaster. Egypt J Genet Cytol. 10:261
93. Meirmans PG. 2012. The trouble with isolation by distance. Mol Ecol. 21:2839-2846
94. Menozzi P, Krimbas CB. 1992. The inversion polymorphism of D. subobscura revisited: synthetic maps of gene arrangement frequencies and their interpretation. J Evol Biol. 5:625-641
95. Mettler LE, Voelker RA, Mukai T. 1977. Inversion clines in populations of Drosophila melanogaster. Genetics 87:169-176
96. Mitrovski P, Hoffmann AA. 2001. Postponed reproduction as an adaptation to winter conditions in Drosophila melanogaster: evidence for clinal variation under semi-natural conditions. Proc R Soc B Biol Sci. 268:2163-2168
97. Mukai T, Voelker RA. 1977. The genetic structure of natural populations of Drosophila melanogaster XIII. Further studies on linkage disequilibrium. Genetics 86:175-185
98. Mukai T, Watanabe TK, Yamaguchi O. 1974. The genetic structure of natural populations of Drosophila melanogaster. XII. Linkage disequilibrium in a large local population. Genetics 77:771-793
99. Navarro A, Barbadilla A, Ruiz A. 2000. Effect of inversion polymorphism on the neutral nucleotide variability of linked chromosomal regions in Drosophila. Genetics 155:685-698
100. Navarro A, Barton NH. 2003. Accumulating postzygotic isolation genes in parapatry: a new twist on chromosomal speciation. Evolution 57:447-459
101. Navarro A, Betrán E, Barbadilla A, Ruiz A. 1997. Recombination and gene flux caused by gene conversion and crossing over in inversion heterokaryotypes. Genetics 146:695-709
102. Noor MA, Grams KL, Bertucci LA, Reiland J. 2001. Chromosomal inversions and the reproductive isolation of species. Proc Natl Acad Sci U S A. 98:12084-12088
103. Orozco-Wengel P, Kapun M, Nolte V, Kofler R, Flatt T, Schlotterer C. 2012. Adaptation of Drosophila to a novel laboratory environment reveals temporally heterogeneous trajectories of selected alleles. Mol Ecol. 21:4931-4941
104. Paaby AB, Bergland AO, Behrman EL, Schmidt PS. 2014. A highly pleiotropic amino acid polymorphism in the Drosophila insulin receptor contributes to life-history adaptation. Evolution 68:3395-3409
105. Paaby AB, Blacket MJ, Hoffmann AA, Schmidt PS. 2010. Identification of a candidate adaptive polymorphism for Drosophila life history by parallel independent clines on two continents. Mol Ecol. 19:760-774
106. Paaby AB, Schmidt PS. 2009. Dissecting the genetics of longevity in Drosophila melanogaster. Fly (Austin) 3:29-38
107. Polechová J, Barton NH. 2015. Limits to adaptation along environmental gradients. Proc Natl Acad Sci U S A. 112:6401-6406
108. Powell JR. 1997. Progress and prospects in evolutionary biology: the Drosophila model. New York: Oxford University Press
109. Rako L, Anderson AR, Sgro CM, Stocker AJ, Hoffmann AA. 2006. The association between inversion In(3R)Payne and clinally varying traits in Drosophila melanogaster. Genetica 128:373-384
110. Rane RV, Rako L, Kapun M, Lee SF, Hoffmann AA. 2015. Genomic evidence for role of inversion 3RP of Drosophila melanogaster in facilitating climate change adaptation. Mol Ecol, 24:2423-2432
111. Reinhardt JA, Kolaczkowski B, Jones CD, Begun DJ, Kern AD. 2014. Parallel geographic variation in Drosophila melanogaster. Genetics 197:361-373
112. Rhomberg LR, Singh RS. 1988. Evidence for a link between local and seasonal cycles in gene frequencies and latitudinal gene clines in a cyclic parthenogen. Genetica 78:73-79
113. Rieseberg LH. 2001. Chromosomal rearrangements and speciation. Trends Ecol Evol. 16:351-358
114. Rodriguez-Trelles F, Alvarez G, Zapata C. 1996. Time-series analysis of seasonal changes of the O inversion polymorphism of Drosophila subobscura. Genetics 142:179-187
115. Rodriguez-Trelles F, Tarrio R, Santos M. 2013. Genome-wide evolutionary response to a heat wave in Drosophila. Biol Lett. 9:20130228
116. Roff D. 1980. Optimizing development time in a seasonal environment: The "ups and downs" of clinal variation. Oecologia 45:202-208
117. Sanchez-Refusta F, Santiago E, Rubio J. 1990. Seasonal fluctuations of cosmopolitan inversion frequencies in a natural population of Drosophila melanogaster. Genet Sel Evol. 22:47-56
118. Santos M, Cespedes W, Balanya J, Trotta V, Calboli FCF, Fontdevila A, Serra L. 2004. Temperature-related genetic changes in laboratory populations of Drosophila subobscura: evidence against simple climatic-based explanations for latitudinal clines. Am Nat. 165: 258-273
119. Schaeffer SW. 2008. Selection in heterogeneous environmentsmaintains the gene arrangement polymorphism of Drosophila pseudoobscura. Evolution 62:3082-3099
120. Schaeffer SW, Goetting-Minesky MP, Kovacevic M, Peoples JR, Graybill JL, Miller JM, Kim K, Nelson JG, Anderson WW. 2003. Evolutionary genomics of inversions in Drosophila pseudoobscura: evidence for epistasis. Proc Natl Acad Sci U S A. 100:8319-8324
121. Schlotterer C, Tobler R, Kofler R, Nolte V. 2014. Sequencing pools of individuals-mining genome-wide polymorphism data without big funding. Nat Rev Genet. 15:749-763
122. Schmidt PS. 2011. Evolution and mechanisms of insect reproductive diapause: a plastic and pleiotropic life history syndrome. In: Flatt T, Heyland A, editors. Mechanisms of life history evolution. The genetics and physiology of life history traits and trade-offs. Oxford: Oxford University Press. p. 230-242
123. Schmidt PS, Matzkin L, Ippolito M, EanesWF. 2005. Geographic variation in diapause incidence, life-history traits, and climatic adaptation in Drosophila melanogaster. Evolution 59:1721-1732
124. Schmidt PS, Paaby AB. 2008. Reproductive diapause and life-history clines in North American populations of Drosophila melanogaster. Evolution 62:1204-1215
125. Schmidt PS, Zhu CT, Das J, Batavia M, Yang L, EanesWF. 2008. An amino acid polymorphism in the couch potato gene forms the basis for climatic adaptation in Drosophila melanogaster. Proc Natl Acad Sci U S A. 105:16207-16211
126. Sezgin E, Duvernell DD, Matzkin LM, Duan Y, Zhu CT, Verrelli BC, Eanes WF. 2004. Single-locus latitudinal clines and their relationship to temperate adaptation in metabolic genes and derived alleles in Drosophila melanogaster. Genetics 168:923-931
127. Sgro CM, van Heerwaarden B, Kellermann V, Wee CW, Hoffmann AA, Lee SF. 2013. Complexity of the genetic basis of ageing in nature revealed by a clinal study of lifespan and methuselah, a gene for ageing, in Drosophila from eastern Australia. Mol Ecol. 22:3539-3551
128. Sperlich D, Pfriem P. 1986. Chromosomal polymorphism in natural and experimental populations. In: M Ashburner, HL Carson, JR Thompson, editors. The genetics and biology of Drosophila. Vol. 3. New York: Academic Press. p. 257-309
129. Stalker HD. 1976. Chromosome studies in wild populations of D. melanogaster. Genetics 82:323-347
130. Stalker HD. 1980. Chromosome studies in wild populations of Drosophila melanogaster. II. Relationship of inversion frequencies to latitude, season, wing-loading and flight activity. Genetics 95: 211-223
131. Stefansson H, Helgason A, Thorleifsson G, Steinthorsdottir V, Masson G, Barnard J, Baker A, Jonasdottir A, Ingason A, Gudnadottir VG, et al. 2005. A common inversion under selection in Europeans. Nat Genet. 37:129-137
132. Sturtevant AH. 1921. A case of rearrangement of genes in Drosophila. Proc Natl Acad Sci U S A. 7:235-237
133. Sturtevant AH, Beadle GW. 1936. The relations of inversions in the X chromosome of Drosophila melanogaster to crossing over and disjunction. Genetics 21:554-604
134. TatarM, Kopelman A, Epstein D, TuMP, Yin CM, Garofalo R. 2001. A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292:107-110
135. Turner TL, Levine MT, Eckert ML, Begun DJ. 2008. Genomic analysis of adaptive differentiation in Drosophila melanogaster. Genetics 179: 455-473
136. Umina PA, Weeks AR, Kearney MR, McKechnie SW, Hoffmann AA. 2005. A rapid shift in a classic clinal pattern in Drosophila reflecting climate change. Science 308:691-693
137. Weeks AR, McKechnie SW, Hoffmann AA. 2002. Dissecting adaptive clinal variation: markers, inversions and size/stress associations in Drosophila melanogaster from a central field population. Ecol Lett. 5:756-763
138. White BJ, Hahn MW, Pombi M, Cassone BJ, Lobo NF, Simard F, Besansky NJ. 2007. Localization of candidate regions maintaining a common polymorphic inversion (2La) in Anopheles gambiae. PLoS Genet. 3:e217
139. Wright S, Dobzhansky T. 1946. Genetics of natural populations. XII. Experimental reproduction of some of the changes caused by natural selection in certain populations of Drosophila pseudoobscura. Genetics 31:125-156
140. Yeaman S. 2013. Genomic rearrangements and the evolution of clusters of locally adaptive loci. Proc Natl Acad Sci U S A 110:E1743-E1751
141. Zhao L, Wit J, Svetec N, Begun DJ. 2015. Parallel gene expression differences between low and high latitude populations of Drosophila melanogaster and D. simulans. PLoS Genet. 11:e1005184
142. Zhu Y, Bergland AO, González J, Petrov DA. 2012. Empirical validation of pooled whole genome population re-sequencing in Drosophila melanogaster. PLoS One 7:e41901