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Genome‐wide patterns of latitudinal differentiation among populations of D rosophila melanogaster from N orth A merica

Daniel K. Fabian, Martin Kapun, Viola Nolte and 4 more

Molecular Ecology · 2012

doi:10.1111/j.1365-294x.2012.05731.x

Abstract

Understanding the genetic underpinnings of adaptive change is a fundamental but largely unresolved problem in evolutionary biology. D rosophila melanogaster , an ancestrally tropical insect that has spread to temperate regions and become cosmopolitan, offers a powerful opportunity for identifying the molecular polymorphisms underlying clinal adaptation. Here, we use genome‐wide next‐generation sequencing of DNA pools (‘pool‐seq’) from three populations collected along the N orth A merican east coast to examine patterns of latitudinal differentiation. Comparing the genomes of these populations is particularly interesting since they exhibit clinal variation in a number of important life history traits. We find extensive latitudinal differentiation, with many of the most strongly differentiated genes involved in major functional pathways such as the insulin/ TOR , ecdysone, torso, EGFR , TGF β/ BMP , JAK / STAT , immunity and circadian rhythm pathways. We observe particularly strong differentiation on chromosome 3R , especially within the cosmopolitan inversion In(3R)Payne , which contains a large number of clinally varying genes. While much of the differentiation might be driven by clinal differences in the frequency of In(3R)P , we also identify genes that are likely independent of this inversion. Our results provide genome‐wide evidence consistent with pervasive spatially variable selection acting on numerous loci and pathways along the well‐known North American cline, with many candidates implicated in life history regulation and exhibiting parallel differentiation along the previously investigated Australian cline.

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References 130

  1. 1.

    Adams MD, Celniker SE, Holt RA, et al. The genome sequence of Drosophila melanogaster. Science. 2000;287:2185-2195.

    Not in our library10.1126/science.287.5461.2185

  2. 2.

    Akey JM. Constructing genomic maps of positive selection in humans: where do we go from here? Genome Research. 2009;19:711-722.

    Not in our library10.1101/gr.086652.108

  3. 3.

    Akey JM, Ruhe AL, Akey DT, et al. Tracking footprints of artificial selection in the dog genome. Proceedings of the National Academy of Sciences USA. 2010;107:1160-1165.

    Not in our library10.1073/pnas.0909918107

  4. 4.

    Anderson AR, Collinge JE, Hoffmann AA, Kellett M, McKechnie SW. Thermal tolerance trade-offs associated with the right arm of chromosome 3 and marked by the hsr-omega gene in Drosophila melanogaster. Heredity. 2003;90:195-202.

    Not in our library10.1038/sj.hdy.6800220

  5. 5.

    Anderson AR, Hoffmann AA, McKechnie SW, Umina PA, Weeks AR. The latitudinal cline in the In(3R)Payne inversion polymorphism has shifted in the last 20 years in Australian Drosophila melanogaster populations. Molecular Ecology. 2005;14:851-858.

    Not in our library10.1111/j.1365-294x.2005.02445.x

  6. 6.

    Ashburner M, Lemeunier F. Relationships within the melanogaster species subgroup of the genus Drosophila (Sophophora). I. Inversion polymorphisms in drosophila melanogaster and Drosophila simulans. Proceedings of the Royal Society of London B. 1976;193:137-157.

    Not in our library10.1098/rspb.1976.0036

  7. 7.

    Ashburner M, Ball CA, Blake JA, et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nature Genetics. 2000;25:25-29.

    Not in our library10.1038/75556

  8. 8.

    Barrett RDH, Hoekstra HE. Molecular spandrels: tests of adaptation at the genetic level. Nature Reviews Genetics. 2011;12:767-780.

    Not in our library10.1038/nrg3015

  9. 9.

    Barton NH. Multilocus clines. Evolution. 1983;37:454-471.

    Not in our library10.1111/j.1558-5646.1983.tb05563.x

  10. 10.

    Barton NH. Clines in polygenic traits. Genetical Research. 1999;74:223-236.

    Not in our library10.1017/s001667239900422x

  11. 11.

    Beaumont MA. Adaptation and speciation: what can FST tell us? Trends in Ecology and Evolution. 2005;20:435-440.

    Not in our library10.1016/j.tree.2005.05.017

  12. 12.

    Beaumont MA, Balding DJ. Identifying adaptive genetic divergence among populations from genome scans. Molecular Ecology. 2004;13:969-980.

    Not in our library10.1111/j.1365-294x.2004.02125.x

  13. 13.

    Begun DJ, Aquadro CF. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature. 1992;356:519-520.

    Not in our library10.1038/356519a0

  14. 14.

    Berry A, Kreitman M. Molecular analysis of an allozyme cline: alcohol dehydrogenase in Drosophila melanogaster on the East Coast of North America. Genetics. 1993;134:869-893.

    Not in our library10.1093/genetics/134.3.869

  15. 15.

    Black WC, Baer CF, Antolin MF, DuTeau NM. Population genomics: genome-wide sampling of insect populations. Annual Review of Entomology. 2001;46:441-469.

    Not in our library10.1146/annurev.ento.46.1.441

  16. 16.

    Bouletreau-Merle J, Fouillet P, Varaldi J. Divergent strategies in low temperature environment for the sibling species Drosophila melanogaster and D. simulans: overwintering in extension border areas of France and comparison with African populations. Evolutionary Ecology. 2003;17:523-548.

    Not in our library

  17. 17.

    Calboli FC, 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;57:2653-2658.

    Not in our library10.1111/j.0014-3820.2003.tb01509.x

  18. 18.

    Caracristi G, Schlötterer C. Genetic differentiation between American and European Drosophila melanogaster populations could be attributed to admixture of African alleles. Molecular Biology and Evolution. 2003;20:792-799.

    Not in our library10.1093/molbev/msg091

  19. 19.

    Charlesworth B, Charlesworth D. Elements of Evolutionary Genetics. 2010.

    Not in our library

  20. 20.

    Cheng C, White BJ, Kamdem C, et al. Ecological genomics of Anopheles gambiae along a latitudinal cline in Cameroon: a population resequencing approach. Genetics. 2012;190:1417-1432.

    Not in our library10.1534/genetics.111.137794

  21. 21.

    Colombani J, Bianchini L, Layalle S, et al. Antagonistic actions of ecdysone and insulins determine final size in Drosophila. Science. 2005;310:667-670.

    Not in our library10.1126/science.1119432

  22. 22.

    Costa R, Peixoto AA, Barbujani G, Kyriacou CP. A latitudinal cline in a Drosophila Clock gene. Proceedings of the Royal Society of London B. 1992;250:43-49.

    Not in our library10.1098/rspb.1992.0128

  23. 23.

    Coyne JA, Beecham E. Heritability of two morphological characters within and among natural populations of Drosophila melanogaster. Genetics. 1987;117:727-737.

    Not in our library10.1093/genetics/117.4.727

  24. 24.

    Cuevas JM, Domingo-Calap P, Sanjuan R. The fitness effects of synonymous mutations in DNA and RNA viruses. Molecular Biology and Evolution. 2011;19:17-20.

    Not in our library10.1093/molbev/msr179

  25. 25.

    Dalmasso C, Broët P, Moreau T. A simple procedure for estimating the false discovery rate. Bioinformatics. 2005;21:660-668.

    Not in our library10.1093/bioinformatics/bti063

  26. 26.

    David JR, Bocquet C. Evolution in a cosmopolitan species: genetic latitudinal clines in Drosophila melanogaster wild populations. Experientia. 1975;31:164-166.

    Not in our library10.1007/bf01990682

  27. 27.

    David JR, Capy P. Genetic variation of Drosophila melanogaster natural populations. Trends in Genetics. 1988;111:357-370.

    Not in our library10.1016/0168-9525(88)90098-4

  28. 28.

    De Jong G, Bochdanovits Z. Latitudinal clines in Drosophila melanogaster: body size, allozyme frequencies, inversion frequencies, and the insulin-signalling pathway. Journal of Genetics. 2003;82:207-223.

    Not in our library10.1007/bf02715819

  29. 29.

    Dobzhansky T. Genetics of the Evolutionary Process. 1970.

    Not in our library

  30. 30.

    Endler JA. Geographic Variation, Speciation and Clines. 1977.

    Not in our library

  31. 31.

    Felsenstein J. The theoretical population genetics of variable selection and migration. Annual Review of Genetics. 1976;10:253-280.

    Not in our library10.1146/annurev.ge.10.120176.001345

  32. 32.

    Ferrandon D, Imler J, Hetru C, Hoffmann J. The Drosophila systemic immune response: sensing and signaling during bacterial and fungal infections. Nature Reviews Immunology. 2007;7:862-874.

    Not in our library10.1038/nri2194

  33. 33.

    Finch CE, Rose MR. Hormones and the physiological architecture of life history evolution. Quarterly Review of Biology. 1995;70:1-52.

    Not in our library10.1086/418864

  34. 34.

    Flatt T, Heyland A. Mechanisms of Life History Evolution. The Genetics and Physiology of Life History Traits and Trade-Offs. 2011.

    Not in our library

  35. 35.

    Flatt T, Heyland A, Rus F, et al. Hormonal regulation of the humoral innate response in Drosophila melanogaster. Journal of Experimental Biology. 2008;211:2712-2724.

    Not in our library10.1242/jeb.014878

  36. 36.

    Futschik A, Schlötterer C. The next generation of molecular markers from massively parallel sequencing of pooled DNA samples. Genetics. 2010;186:207-218.

    Not in our library10.1534/genetics.110.114397

  37. 37.

    Galikova M, Klepsatel P, Senti G, Flatt T. Steroid hormone regulation of C. elegans and Drosophila aging and life history. Experimental Gerontology. 2011;46:141-147.

    Not in our library10.1016/j.exger.2010.08.021

  38. 38.

    Giannakou ME, Partridge L. Role of insulin-like signalling in Drosophila lifespan. Trends in Biochemical Science. 2007;32:180-188.

    Not in our library10.1016/j.tibs.2007.02.007

  39. 39.

    Gockel J, Kennington WJ, Hoffmann AA, Goldstein DB, Partridge L. Nonclinality of molecular variation implicates selection in maintaining a morphological cline of Drosophila melanogaster. Genetics. 2001;158:319-323.

    Not in our library10.1093/genetics/158.1.319

  40. 40.

    Gockel J, Robinson SJ, Kennington WJ, Goldstein DB, Partridge L. Quantitative genetic analysis of natural variation in body size in Drosophila melanogaster. Heredity. 2002;89:145-153.

    Not in our library10.1038/sj.hdy.6800121

All 130 references

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