Skip to content
naulon
Get started

No retraction, correction or concern found when last checked on Oct 17, 2026.

Genomic Evidence of Rapid and Stable Adaptive Oscillations over Seasonal Time Scales in Drosophila

Alan O. Bergland, Emily L. Behrman, Katherine R. O'Brien and 2 more (opens in a new tab)

PLoS Genetics · 2014

doi:10.1371/journal.pgen.1004775 (opens in a new tab)

Abstract

In many species, genomic data have revealed pervasive adaptive evolution indicated by the fixation of beneficial alleles. However, when selection pressures are highly variable along a species' range or through time adaptive alleles may persist at intermediate frequencies for long periods. So called "balanced polymorphisms" have long been understood to be an important component of standing genetic variation, yet direct evidence of the strength of balancing selection and the stability and prevalence of balanced polymorphisms has remained elusive. We hypothesized that environmental fluctuations among seasons in a North American orchard would impose temporally variable selection on Drosophila melanogaster that would drive repeatable adaptive oscillations at balanced polymorphisms. We identified hundreds of polymorphisms whose frequency oscillates among seasons and argue that these loci are subject to strong, temporally variable selection. We show that these polymorphisms respond to acute and persistent changes in climate and are associated in predictable ways with seasonally variable phenotypes. In addition, our results suggest that adaptively oscillating polymorphisms are likely millions of years old, with some possibly predating the divergence between D. melanogaster and D. simulans. Taken together, our results are consistent with a model of balancing selection wherein rapid temporal fluctuations in climate over generational time promotes adaptive genetic diversity at loci underlying polygenic variation in fitness related phenotypes.

Full text

Its licence does not allow us to show the full text. Read it at PubMed Central:

Read at PubMed Central (opens in a new tab)

References 128

  1. 1.

    Gillespie JH (1973 ) Polymorphism in Random Environments. Theoretical Population Biology 4: 193–195.

    Not in our library

  2. 2.

    Ellner S, Sasaki A (1996 ) Patterns of genetic polymorphism maintained by fluctuating selection with overlapping generations. Theor Popul Biol 50: 31–65.

    Not in our library10.1006/tpbi.1996.0022 (opens in a new tab)

  3. 3.

    Korol AB, Kirzhner VM, Ronin YI, Nevo E (1996 ) Cyclical environmental changes as a factor maintaining genetic polymorphism. 2. Diploid selection for an additive trait. Evolution 50: 1432–1441.

    Not in our library10.1111/j.1558-5646.1996.tb03917.x (opens in a new tab)

  4. 4.

    Ewing EP (1979 ) Genetic-Variation in a Heterogeneous Environment. 7. Temporal and Spatial Heterogeneity in Infinite Populations. American Naturalist 114: 197–212.

    Not in our library

  5. 5.

    Gillespie JH, Langley CH (1974 ) General Model to Account for Enzyme Variation in Natural-Populations. Genetics 76: 837–884.

    Not in our library10.1093/genetics/76.4.837 (opens in a new tab)

  6. 6.

    Hoekstra RF (1978 ) Sufficient Conditions for Polymorphism with Cyclical Selection in a Subdivided Population. Genetical Research 31: 67–73.

    Not in our library

  7. 7.

    Haldane JBS, Jayakar SD (1962 ) Polymorphism Due to Selection of Varying Direction. Journal of Genetics 58: 237–242.

    Not in our library

  8. 8.

    Hedrick PW (1976 ) Genetic-Variation in a Heterogeneous Environment. 2. Temporal Heterogeneity and Directional Selection. Genetics 84: 145–157.

    Not in our library10.1093/genetics/84.1.145 (opens in a new tab)

  9. 9.

    Gershenson S (1945 ) Evolutionary Studies on the Distribution and Dynamics of Melanism in the Hamster (Cricetus cricetus L). 1. Distribution of Black Hamsters in the Ukrainian and Bashkirian Soviet Socialist Republics (USSR). Genetics 30: 207–232.

    Not in our library10.1093/genetics/30.3.207 (opens in a new tab)

  10. 10.

    Grant PR, Grant BR (2002 ) Unpredictable evolution in a 30-year study of Darwin's finches. Science 296: 707–711.

    Not in our library10.1126/science.1070315 (opens in a new tab)

  11. 11.

    Tarwater CE, Beissinger SR (2013 ) Opposing selection and environmental variation modify optimal timing of breeding. Proc Natl Acad Sci U S A 110: 15365–15370.

    Not in our library10.1073/pnas.1303821110 (opens in a new tab)

  12. 12.

    Brown CR, Brown MB, Roche EA (2013 ) Fluctuating viability selection on morphology of cliff swallows is driven by climate. J Evol Biol 26: 1129–1142.

    Not in our library10.1111/jeb.12130 (opens in a new tab)

  13. 13.

    Wall S, Carter MA, Clarke B (1980 ) Temporal Changes of Gene-Frequencies in Cepaea hortensis. Biological Journal of the Linnean Society 14: 303–317.

    Not in our library

  14. 14.

    Brakefield PM (1985 ) Differential Winter Mortality and Seasonal Selection in the Polymorphic Ladybird Adalia bipunctata (L) in the Netherlands. Biological Journal of the Linnean Society 24: 189–206.

    Not in our library

  15. 15.

    Hairston NG, Dillon TA (1990 ) Fluctuating Selection and Response in a Population of Fresh-Water Copepods. Evolution 44: 1796–1805.

    Not in our library10.1111/j.1558-5646.1990.tb05250.x (opens in a new tab)

  16. 16.

    Bradshaw WE (1973 ) Homeostasis and Polymorphism in Vernal Development of Chaoborus americanus. Ecology 54: 1247–1259.

    Not in our library

  17. 17.

    Vavrek MC, McGraw JB, Yang HS (1996 ) Within-population variation in demography of Taraxacum officinale: Maintenance of genetic diversity. Ecology 77: 2098–2107.

    Not in our library

  18. 18.

    Axenovich TI, Zorkoltseva IV, Akberdin IR, Beketov SV, Kashtanov SN, et al (2007 ) Inheritance of litter size at birth in farmed arctic foxes (Alopex lagopus, Canidae, Carnivora). Heredity 98: 99–105.

    Not in our library10.1038/sj.hdy.6800908 (opens in a new tab)

  19. 19.

    Vorburger C (2006 ) Temporal dynamics of genotypic diversity reveal strong clonal selection in the aphid Myzus persicae. Journal of Evolutionary Biology 19: 97–107.

    Not in our library10.1111/j.1420-9101.2005.00985.x (opens in a new tab)

  20. 20.

    Niklasson M, Tomiuk J, Parker ED (2004 ) Maintenance of clonal diversity in Dipsa bifurcata (Fallen, 1810) (Diptera: Lonchopteridae). I. Fluctuating seasonal selection moulds long-term coexistence. Heredity 93: 62–71.

    Not in our library10.1038/sj.hdy.6800480 (opens in a new tab)

  21. 21.

    Tomiuk J, Niklasson M, Parker ED (2004 ) Maintenance of clonal diversity in Dipsa bifurcata (Fallen, 1810) (Diptera: Lonchopteridae). II. Diapause stabilizes clonal coexistence. Heredity 93: 72–77.

    Not in our library10.1038/sj.hdy.6800481 (opens in a new tab)

  22. 22.

    Templeton A, Johnston JS (1982) Life history evolution under pleiotropy and K-selection in a natural population of Drosophila mercatorum. In: Barker JSF, Starmer WT, editors. Ecological Genetics and Evolution: The Cactus-Yeast-Drosophila Model System. New York: Academic Press. pp. 225–239.

    Not in our library

  23. 23.

    Hart-Schmidt RA (2012 ) Geographically patterned variation in diapause and its relationship to other climate-associated phenotypes and genotypes of Drosophila americana: University of Iowa.

    Not in our library

  24. 24.

    Rodriguez-Trelles F, Tarrio R, Santos M (2013 ) Genome-wide evolutionary response to a heat wave in Drosophila. Biol Lett 9: 20130228.

    Not in our library10.1098/rsbl.2013.0228 (opens in a new tab)

  25. 25.
    Fluctuating selection: the perpetual renewal of adaptation in variable environments · 2010
    No notice
  26. 26.

    Siepielski AM, DiBattista JD, Carlson SM (2009 ) It's about time: the temporal dynamics of phenotypic selection in the wild. Ecol Lett 12: 1261–1276.

    Not in our library10.1111/j.1461-0248.2009.01381.x (opens in a new tab)

  27. 27.

    Dobzhansky T (1943 ) Genetics of Natural Populations. IX. Temporal Changes in the Composition of Populations of Drosophila pseudoobscura. Genetics 28: 162–186.

    Not in our library10.1093/genetics/28.2.162 (opens in a new tab)

  28. 28.

    Dobzhansky T, Ayala FJ (1973 ) Temporal Frequency Changes of Enzyme and Chromosomal Polymorphisms in Natural Populations of Drosophila. Proceedings of the National Academy of Sciences of the United States of America 70: 680–683.

    Not in our library10.1073/pnas.70.3.680 (opens in a new tab)

  29. 29.

    Mueller LD, Barr LG, Ayala FJ (1985 ) Natural-Selection vs Random Drift - Evidence from Temporal Variation in Allele Frequencies in Nature. Genetics 111: 517–554.

    Not in our library10.1093/genetics/111.3.517 (opens in a new tab)

  30. 30.

    Nielsen KM, Hoffmann AA, Mckechnie SW (1985 ) Population-Genetics of the Metabolically Related Adh, Gpdh and Tpi Polymorphisms in Drosophila melanogaster. 2. Temporal and Spatial Variation in an Orchard Population. Genetics Selection Evolution 17: 41–58.

    Not in our library10.1186/1297-9686-17-1-41 (opens in a new tab)

  31. 31.

    Knibb WR (1986 ) Temporal Variation of Drosophila melanogaster Adh Allele Frequencies, Inversion Frequencies, and Population Sizes. Genetica 71: 175–190.

    Not in our library

  32. 32.

    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.

    Not in our library10.1093/genetics/142.1.179 (opens in a new tab)

  33. 33.

    Ananina G, Peixoto AA, Bitner-Mathe BC, Souza WN, da Silva LB, et al (2004 ) Chromosomal inversion polymorphism in Drosophila mediopunctata: seasonal, altitudinal, and latitudinal variation. Genetics and Molecular Biology 27: 61–69.

    Not in our library

  34. 34.

    Bouletreaumerle J, Fouillet P, Terrier O (1992 ) Clinal and Seasonal-Variations in Initial Retention Capacity of Virgin Drosophila melanogaster Females as a Strategy for Fitness. Evolutionary Ecology 6: 223–242.

    Not in our library

  35. 35.

    Schmidt PS, Conde DR (2006 ) Environmental heterogeneity and the maintenance of genetic variation for reproductive diapause in Drosophila melanogaster. Evolution 60: 1602–1611.

    Not in our library

  36. 36.

    Stalker HD, Carson HL (1949 ) Seasonal Variation in the Morphology of Drosophila robusta Sturtevant. Evolution 3: 330–343.

    Not in our library10.1111/j.1558-5646.1949.tb00034.x (opens in a new tab)

  37. 37.

    Tantawy AO (1964 ) Studies on Natural-Populations of Drosophila. 3. Morphological and Genetic-Differences of Wing Length in Drosophila melanogaster and Drosophila simulans in Relation to Season. Evolution 18: 560–570.

    Not in our library

  38. 38.

    Miyo T, Akai S, Oguma Y (2000 ) Seasonal fluctuation in susceptibility to insecticides within natural populations of Drosophila melanogaster: empirical observations of fitness costs of insecticide resistance. Genes & Genetic Systems 75: 97–104.

    Not in our library10.1266/ggs.75.97 (opens in a new tab)

  39. 39.

    Dev K, Chahal J, Parkash R, Kataria SK (2013 ) Correlated Changes in Body Melanisation and Mating Traits of Drosophila melanogaster: A Seasonal Analysis. Evolutionary Biology 40: 366–376.

    Not in our library

  40. 40.

    Gillespie GH (2000 ) Genetic Drift in an Infinite Population: The Pseudohitchhiking Model. Genetics 155: 909–919.

    Not in our library10.1093/genetics/155.2.909 (opens in a new tab)

  41. 41.

    Wright S (1943 ) Isolation by Distance. Genetics 28: 114–138.

    Not in our library10.1093/genetics/28.2.114 (opens in a new tab)

  42. 42.

    Zhu Y, Bergland AO, Gonzalez J, Petrov DA (2012 ) Empirical Validation of Pooled Whole Genome Population Re-Sequencing in Drosophila melanogaster. PLoS One 7: e41901.

    Not in our library10.1371/journal.pone.0041901 (opens in a new tab)

  43. 43.
    Strong Purifying Selection at Synonymous Sites in D. melanogaster · 2013
    No notice
  44. 44.

    Pechmann S, Frydman J (2013 ) Evolutionary conservation of codon optimality reveals hidden signatures of cotranslational folding. Nat Struct Mol Biol 20: 237–243.

    Not in our library10.1038/nsmb.2466 (opens in a new tab)

  45. 45.

    Mackay TF, Richards S, Stone EA, Barbadilla A, Ayroles JF, et al (2012 ) The Drosophila melanogaster Genetic Reference Panel. Nature 482: 173–178.

    Not in our library10.1038/nature10811 (opens in a new tab)

  46. 46.

    Kapun M, van Schalkwyk H, McAllister B, Flatt T, Schlotterer C (2014 ) Inference of chromosomal inversion dynamics from Pool-Seq data in natural and laboratory populations of Drosophila melanogaster. Molecular Ecology 23: 1813–1827.

    Not in our library10.1111/mec.12594 (opens in a new tab)

  47. 47.
    Population Genomics of Inversion Polymorphisms in Drosophila melanogaster · 2012
    Corrected
  48. 48.

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

    Not in our library10.1554/0014-3820(2001)055[1063:cctamc]2.0.co;2 (opens in a new tab)

  49. 49.

    Karan D, Dahiya N, Munjal AK, Gibert P, Moreteau B, et al (1998 ) Desiccation and starvation tolerance of adult Drosophila: Opposite latitudinal clines in natural populations of three different species. Evolution 52: 825–831.

    Not in our library10.1111/j.1558-5646.1998.tb03706.x (opens in a new tab)

  50. 50.

    Kenny MC, Wilton A, Ballard JWO (2008 ) Seasonal trade-off between starvation resistance and cold resistance in temperate wild-caught Drosophila simulans. Australian Journal of Entomology 47: 20–23.

    Not in our library

  51. 51.

    Parkash R, Sharma V, Kalra B (2009 ) Impact of body melanisation on desiccation resistance in montane populations of D. melanogaster: Analysis of seasonal variation. Journal of Insect Physiology 55: 898–908.

    Not in our library10.1016/j.jinsphys.2009.06.004 (opens in a new tab)

  52. 52.

    Schmidt PS, Paaby AB, Heschel MS (2005 ) Genetic variance for diapause expression and associated life histories in Drosophila melanogaster. Evolution 59: 2616–2625.

    Not in our library

  53. 53.

    Sisodia S, Singh BN (2010 ) Resistance to environmental stress in Drosophila ananassae: latitudinal variation and adaptation among populations. Journal of Evolutionary Biology 23: 1979–1988.

    Not in our library10.1111/j.1420-9101.2010.02061.x (opens in a new tab)

  54. 54.

    Huang W, Richards S, Carbone MA, Zhu DH, Anholt RRH, et al (2012 ) Epistasis dominates the genetic architecture of Drosophila quantitative traits. Proceedings of the National Academy of Sciences of the United States of America 109: 15553–15559.

    Not in our library10.1073/pnas.1213423109 (opens in a new tab)

  55. 55.
    Population Genomics of Sub-Saharan Drosophila melanogaster: African Diversity and Non-African Admixture · 2012
    No notice
  56. 56.

    Klein J, Sato A, Nagl S, O'hUigin C (1998 ) Molecular trans-species polymorphism. Annual Review of Ecology and Systematics 29: 1–21.

    Not in our library

  57. 57.

    Leffler EM, Gao Z, Pfeifer S, Segurel L, Auton A, et al (2013 ) Multiple instances of ancient balancing selection shared between humans and chimpanzees. Science 339: 1578–1582.

    Not in our library10.1126/science.1234070 (opens in a new tab)

  58. 58.

    Welbergen P, van Dijken FR, Scharloo W, Kohler W (1992 ) The genetic basis of sexual isolation between Drosophila melanogaster and D. simulans. Evolution 46: 1385–1398.

    Not in our library10.1111/j.1558-5646.1992.tb01131.x (opens in a new tab)

  59. 59.

    Sturtevant AH (1920 ) Genetic studies on Drosophila simulans. I. Introduction. Hybrids with Drosophila melanogaster. Genetics 5: 488–500.

    Not in our library10.1093/genetics/5.5.488 (opens in a new tab)

  60. 60.

    Tamura K, Subramanian S, Kumar S (2004 ) Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. Mol Biol Evol 21: 36–44.

    Not in our library10.1093/molbev/msg236 (opens in a new tab)

  61. 61.

    Band HT, Ives PT (1963 ) Genetic-Structure of Populations. 1. Nature of Genetic Load in South Amherst Population of Drosophila melanogaster. Evolution 17: 198–215.

    Not in our library

  62. 62.

    Ives PT, Band HT (1986 ) Continuing Studies on the South Amherst Drosophila melanogaster Natural Population during the 1970s and 1980s. Evolution 40: 1289–1302.

    Not in our library10.1111/j.1558-5646.1986.tb05752.x (opens in a new tab)

  63. 63.

    Messer PW (2013 ) SLiM: Simulating Evolution with Selection and Linkage. Genetics 194: 1037–1039.

    Not in our library10.1534/genetics.113.152181 (opens in a new tab)

  64. 64.
    The Many Landscapes of Recombination in Drosophila melanogaster · 2012
    No notice
  65. 65.

    Schmidt PS, Conde DR (2006 ) Environmental heterogeneity and the maintenance of genetic variation for reproductive diapause in Drosophila melanogaster. Evolution 60: 1602–1611.

    Not in our library

  66. 66.

    Ives PT (1970 ) Futher genetic studies on the South Amherst population of Drosophila melanogaster. Evolution 24: 507–518.

    Not in our library10.1111/j.1558-5646.1970.tb01785.x (opens in a new tab)

  67. 67.

    Coyne JA, Milstead B (1987 ) Long-Distance Migration of Drosophila. 3. Dispersal of Drosophila melanogaster Alleles from a Maryland Orchard. American Naturalist 130: 70–82.

    Not in our library

  68. 68.

    Umina PA (2005 ) A rapid shift in a classic clinal pattern in Drosophila reflecting climate change. Nature 308: 691–693.

    Not in our library10.1126/science.1109523 (opens in a new tab)

  69. 69.

    Berry A, Kreitman M (1993 ) Molecular analysis of an allozyme cline: alcohol dehydrogenase in Drosophila melanogaster on the east coast of North America. Genetics 134: 869–893.

    Not in our library10.1093/genetics/134.3.869 (opens in a new tab)

  70. 70.
    Evidence that Adaptation in Drosophila Is Not Limited by Mutation at Single Sites · 2010
    No notice
  71. 71.

    Mckenzie JA (1980 ) An Ecological Study of the Alcohol-Dehydrogenase (Adh) Polymorphism of Drosophila melanogaster. Australian Journal of Zoology 28: 709–716.

    Not in our library

  72. 72.

    McInnis DO, Schaffer HE, Mettler LE (1982 ) Field Dispersal and Population Sizes of Native Drosophila from North-Carolina. American Naturalist 119: 319–330.

    Not in our library

  73. 73.

    Powell J (1997) Progress and prospects in evolutionary biology: The Drosophila Model. New York: Oxford University Press.

    Not in our library

  74. 74.

    Gravot E, Huet M, Veuille M (2004 ) Effect of breeding structure on population genetic parameters in Drosophila. Genetics 166: 779–788.

    Not in our library10.1093/genetics/166.2.779 (opens in a new tab)

  75. 75.
    A Genome-Wide, Fine-Scale Map of Natural Pigmentation Variation in Drosophila melanogaster · 2013
    No notice
  76. 76.

    Kirkpatrick M (2000 ) Reinforcement and divergence under assortative mating. Proceedings of the Royal Society B-Biological Sciences 267: 1649–1655.

    Not in our library10.1098/rspb.2000.1191 (opens in a new tab)

  77. 77.

    Lewontin RC (1964 ) The Interaction of Selection and Linkage. I. General Considerations; Heterotic Models. Genetics 49: 49–67.

    Not in our library10.1093/genetics/49.1.49 (opens in a new tab)

  78. 78.

    Giesel JT (1977 ) A model of functional epistasis and linkage disequilibrium in populations with overlapping generations. Genetics 86: 679–686.

    Not in our library10.1093/genetics/86.3.679 (opens in a new tab)

  79. 79.

    Lewontin RC (1965) Selection for colonizing ability. In: Baker HG, Stebbins GL, editors. The Genetics of Colonizing Species First International Union of Biological Sciences Symposia on General Biology, Aslimoar, Calif, 1964. New York: Academic Press. pp. 77–94.

    Not in our library

  80. 80.

    Schmidt PS, Paaby AB (2008 ) Reproductive diapause and life-history clines in North American populations of Drosophila melanogaster. Evolution 62: 1204–1215.

    Not in our library10.1111/j.1558-5646.2008.00351.x (opens in a new tab)

  81. 81.

    Schmidt PS, Matzkin L, Ippolito M, Eanes WF (2005 ) Geographic variation in diapause incidence, life-history traits, and climatic adaptation in Drosophila melanogaster. Evolution 59: 1721–1732.

    Not in our library

  82. 82.

    Arthur AL, Weeks AR, Sgro CM (2008 ) Investigating latitudinal clines for life history and stress resistance traits in Drosophila simulans from eastern Australia. Journal of Evolutionary Biology 21: 1470–1479.

    Not in our library10.1111/j.1420-9101.2008.01617.x (opens in a new tab)

  83. 83.

    James AC, Azevedo RB, Partridge L (1997 ) Genetic and environmental responses to temperature of Drosophila melanogaster from a latitudinal cline. Genetics 146: 881–890.

    Not in our library10.1093/genetics/146.3.881 (opens in a new tab)

  84. 84.

    Robinson SJ, Zwaan B, Partridge L (2000 ) Starvation resistance and adult body composition in a latitudinal cline of Drosophila melanogaster. Evolution 54: 1819–1824.

    Not in our library10.1111/j.0014-3820.2000.tb00726.x (opens in a new tab)

  85. 85.

    Lazzaro BP, Flores HA, Lorigan JG, Yourth CP (2008 ) Genotype-by-environment interactions and adaptation to local temperature affect immunity and fecundity in Drosophila melanogaster. PLoS Pathogens 4: e1000025.

    Not in our library10.1371/journal.ppat.1000025 (opens in a new tab)

  86. 86.

    Singh RS, Long AD (1992 ) Geographic variation in Drosophila: From molecules to morphology and back. Trends Ecol Evol 7: 340–345.

    Not in our library10.1016/0169-5347(92)90127-w (opens in a new tab)

  87. 87.

    Ayrinhac A, Debat V, Gibert P, Kister AG, Legout H, et al (2004 ) Cold adaptation in geographical populations of Drosophila melanogaster: phenotypic plasticity is more important than genetic variability. Functional Ecology 18: 700–706.

    Not in our library

  88. 88.

    Hoffmann AA, Anderson A, Hallas R (2002 ) Opposing clines for high and low temperature resistance in Drosophila melanogaster. Ecology Letters 5: 614–618.

    Not in our library

  89. 89.

    Overgaard J, Kristensen TN, Mitchell KA, Hoffmann AA (2011 ) Thermal Tolerance in Widespread and Tropical Drosophila Species: Does Phenotypic Plasticity Increase with Latitude? American Naturalist 178: S80–S96.

    Not in our library10.1086/661780 (opens in a new tab)

  90. 90.

    Hoffmann AA, Harshman LG (1999 ) Desiccation and starvation resistance in Drosophila: patterns of variation at the species, population and intrapopulation levels. Heredity 83: 637–643.

    Not in our library10.1046/j.1365-2540.1999.00649.x (opens in a new tab)

  91. 91.

    Gilchrist GW, Jeffers LM, West B, Folk DG, Suess J, et al (2008 ) Clinal patterns of desiccation and starvation resistance in ancestral and invading populations of Drosophila subobscura. Evolutionary Applications 1: 513–523.

    Not in our library10.1111/j.1752-4571.2008.00040.x (opens in a new tab)

  92. 92.

    Ayroles JF, Carbone MA, Stone EA, Jordan KW, Lyman RF, et al (2009 ) Systems genetics of complex traits in Drosophila melanogaster. Nature Genetics 41: 299–307.

    Not in our library10.1038/ng.332 (opens in a new tab)

  93. 93.

    Reynolds LA (2013) The effects of starvation selection on Drosophila melanogaster life history and development. PhD dissertation, UNLV.

    Not in our library

  94. 94.

    David JR, Capy P (1988 ) Genetic-Variation of Drosophila melanogaster Natural-Populations. Trends in Genetics 4: 106–111.

    Not in our library10.1016/0168-9525(88)90098-4 (opens in a new tab)

  95. 95.

    Sezgin E, Duvernell DD, Matzkin LM, Duan Y, Zhu CT, et al (2004 ) Single-locus latitudinal clines and their relationship to temperate adaptation in metabolic genes and derived alleles in Drosophila melanogaster. Genetics 168: 923–931.

    Not in our library10.1534/genetics.104.027649 (opens in a new tab)

  96. 96.

    Langley CH, Stevens K, Cardeno C, Lee YC, Schrider DR, et al (2012 ) Genomic variation in natural populations of Drosophila melanogaster. Genetics 192: 533–598.

    Not in our library10.1534/genetics.112.142018 (opens in a new tab)

  97. 97.

    Ellner S, Hairston N (1994 ) Role of overlapping generations in maintaining genetic variation in a fluctuating environment. The American Naturalist 143: 403–417.

    Not in our library

  98. 98.

    Garcia-Dorado A (1986 ) The effect of niche preference on polymorphism protection in a hetergeneous environment. Evolution 40: 936–945.

    Not in our library10.1111/j.1558-5646.1986.tb00562.x (opens in a new tab)

  99. 99.

    Hedrick PW (1990) Theoretical analysis of habitat selection and the maintenance of genetic variation. In: Barker JSF, Starmer WT, MacIntyre RJ, editors. Ecological and Evolutionary Genetics of Drosophila. US: Plenum Press. pp. 209–227.

    Not in our library

  100. 100.

    Bergland AO, Chae H-s, Kim Y-J, Tatar M (2012 ) Fine-Scale Mapping of Natural Variation in Fly Fecundity Identifies Neuronal Domain of Expression and Function of an Aquaporin. PLoS Genet 8: e1002631.

    Not in our library10.1371/journal.pgen.1002631 (opens in a new tab)

  101. 101.

    McKechnie SW, Geer BW (1993 ) Micro-evolution in a wine cellar: an historical perspecitve. Genetica 90: 201–215.

    Not in our library10.1007/bf01435040 (opens in a new tab)

  102. 102.

    Rashkovetsky E, Iliadi K, Michalak P, Lupu A, Nevo E, Feder ME, Korol A (2006 ) Adaptive differentiation of thermotolerance in Drosophila along a microclimatic gradient. Heredity 96: 353–359.

    Not in our library10.1038/sj.hdy.6800784 (opens in a new tab)

  103. 103.

    Turelli M, Coyne JA, Prout T (1984 ) Resource choice in orchard populations of Drosophila. Biol J Linn Soc 22: 95–106.

    Not in our library

  104. 104.

    Hoffmann A, O'Donnell S (1990) Heritable variation in resource use in Drosophila in the field. In: Barker JSF, Starmer WT, MacIntyre RJ, editors. Ecological and Evolutionary Genetics of Drosophila. US: Plenum Press. pp. 177–193.

    Not in our library

  105. 105.

    Wallace B (1966 ) Distance and the allelism of lethals in a tropical population of Drosophila melanogaster. The American Naturalist 100: 565–578.

    Not in our library

  106. 106.

    Oshima C (1970 ) Frequencies of intra- and interpopulation allelism of lethals in the several natural populations and the relationship between the dispersal of flies and the frequency of allelism of lethals in natural populations. Drosophila Information Service 45: 167–168.

    Not in our library

  107. 107.

    Capy P, Gibert P, Boussy I (1992) Drosophila melanogaster, Drosophila simulans: so similar, so different. USA: Kluwer Academic Publishers. 292 p.

    Not in our library

  108. 108.

    Ginzburg L, Colyvan M (2003) Ecological orbits: How planets move and populations grow. New York: Oxford University Press.

    Not in our library

  109. 109.

    Li H, Durbin R (2009 ) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754–1760.

    Not in our library10.1093/bioinformatics/btp324 (opens in a new tab)

  110. 110.

    Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al (2009 ) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078–2079.

    Not in our library10.1093/bioinformatics/btp352 (opens in a new tab)

  111. 111.

    McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, et al (2010 ) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20: 1297–1303.

    Not in our library10.1101/gr.107524.110 (opens in a new tab)

  112. 112.

    Bansal V (2010 ) A statistical method for the detection of variants from next-generation resequencing of DNA pools. Bioinformatics 26: i318–324.

    Not in our library10.1093/bioinformatics/btq214 (opens in a new tab)

  113. 113.

    Cingolani P, Platts A, Wang le L, Coon M, Nguyen T, et al (2012 ) A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6: 80–92.

    Not in our library10.4161/fly.19695 (opens in a new tab)

  114. 114.

    Nei M (1987) Molecular Evolutionary Genetics. New York: Columbia University Press.

    Not in our library

  115. 115.

    Kolaczkowski B, Kern AD, Holloway AK, Begun DJ (2010 ) Genomic Differentiation Between Temperate and Tropical Australian Populations of Drosophila melanogaster. Genetics 187: 245–260.

    Not in our library10.1534/genetics.110.123059 (opens in a new tab)

  116. 116.

    Feder AF, Petrov DA, Bergland AO (2012 ) LDx: Estimation of Linkage Disequilibrium from High-Throughput Pooled Resequencing Data. PLoS One 7: e48588.

    Not in our library10.1371/journal.pone.0048588 (opens in a new tab)

  117. 117.

    R Core Development Team (2009) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

    Not in our library

  118. 118.

    Bates D, Maechler M, Bolker B (2011) lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-42. http://CRAN.R-project.org/package=lme4

    Not in our library

  119. 119.

    Højsgaard S, Halekoh U, Yan J (2006 ) The R Package geepack for Generalized Estimating Equations. Journal of Statistical Software 15: 1–11.

    Not in our library

  120. 120.

    Benjamini Y, Hochberg Y (1995 ) Controlling the false discovery rate: a practical and powerful approach ot multiple testing. Journal of the Royal Statistical Society B 57: 289–300.

    Not in our library

  121. 121.

    Ewens WJ (2004) Mathematical Population Genetics. I. Theoretical introduction. Springer-Verlag, New York, NY.

    Not in our library

  122. 122.

    Kleiber C, Zeileis A (2008) Applied econometrics with R. Springer-Verlag, New York, NY.

    Not in our library

  123. 123.

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

    Not in our library10.1038/356519a0 (opens in a new tab)

  124. 124.
    Population Genomics: Whole-Genome Analysis of Polymorphism and Divergence in Drosophila simulans · 2007
    No notice
  125. 125.

    Hu TT, Eisen MB, Thornton KR, Andolfatto P (2013 ) A second-generation assembly of the Drosophila simulans genome provides new insights into patterns of lineage-specific divergence. Genome Research 23: 89–98.

    Not in our library10.1101/gr.141689.112 (opens in a new tab)

  126. 126.

    Harris RS (2007 ) Improved pairwise alignment of genomic DNA: The Pennsylvania State University.

    Not in our library

  127. 127.

    Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, et al (2002 ) The human genome browser at UCSC. Genome Research 12: 996–1006.

    Not in our library10.1101/gr.229102 (opens in a new tab)

  128. 128.

    Paradis E, Claude J, Strimmer K (2004 ) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289–290.

    Not in our library10.1093/bioinformatics/btg412 (opens in a new tab)

Cited by papers we hold 9

Questions about this paper

We email you if it is retracted, withdrawn, corrected or flagged.

Reads

Read by people on this page

None yet.

Checked or read by AI through naulon

None yet.

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.

Are you an author?

Is this your paper?

Claim it to add your note and be paid when agents cite it. Free.