Population Genomics of Inversion Polymorphisms in
Chromosomal inversions have been an enduring interest of population geneticists since their discovery in Drosophila melanogaster. Numerous lines of evidence suggest powerful selective pressures govern the distributions of polymorphic inversions, and these observations have spurred the development of many explanatory models. However, due to a paucity of nucleotide data, little progress has been made towards investigating selective hypotheses or towards inferring the genealogical histories of inversions, which can inform models of inversion evolution and suggest selective mechanisms. Here, we utilize population genomic data to address persisting gaps in our knowledge of D. melanogaster's inversions. We develop a method, termed Reference-Assisted Reassembly, to assemble unbiased, highly accurate sequences near inversion breakpoints, which we use to estimate the age and the geographic origins of polymorphic inversions. We find that inversions are young, and most are African in origin, which is consistent with the demography of the species. The data suggest that inversions interact with polymorphism not only in breakpoint regions but also chromosome-wide. Inversions remain differentiated at low levels from standard haplotypes even in regions that are distant from breakpoints. Although genetic exchange appears fairly extensive, we identify numerous regions that are qualitatively consistent with selective hypotheses. Finally, we show that In(1)Be, which we estimate to be ∼60 years old (95% CI 5.9 to 372.8 years), has likely achieved high frequency via sex-ratio segregation distortion in males. With deeper sampling, it will be possible to build on our inferences of inversion histories to rigorously test selective models—particularly those that postulate that inversions achieve a selective advantage through the maintenance of co-adapted allele complexes.
Vyšlo v časopise:
Population Genomics of Inversion Polymorphisms in. PLoS Genet 8(12): e32767. doi:10.1371/journal.pgen.1003056
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1003056
Souhrn
Chromosomal inversions have been an enduring interest of population geneticists since their discovery in Drosophila melanogaster. Numerous lines of evidence suggest powerful selective pressures govern the distributions of polymorphic inversions, and these observations have spurred the development of many explanatory models. However, due to a paucity of nucleotide data, little progress has been made towards investigating selective hypotheses or towards inferring the genealogical histories of inversions, which can inform models of inversion evolution and suggest selective mechanisms. Here, we utilize population genomic data to address persisting gaps in our knowledge of D. melanogaster's inversions. We develop a method, termed Reference-Assisted Reassembly, to assemble unbiased, highly accurate sequences near inversion breakpoints, which we use to estimate the age and the geographic origins of polymorphic inversions. We find that inversions are young, and most are African in origin, which is consistent with the demography of the species. The data suggest that inversions interact with polymorphism not only in breakpoint regions but also chromosome-wide. Inversions remain differentiated at low levels from standard haplotypes even in regions that are distant from breakpoints. Although genetic exchange appears fairly extensive, we identify numerous regions that are qualitatively consistent with selective hypotheses. Finally, we show that In(1)Be, which we estimate to be ∼60 years old (95% CI 5.9 to 372.8 years), has likely achieved high frequency via sex-ratio segregation distortion in males. With deeper sampling, it will be possible to build on our inferences of inversion histories to rigorously test selective models—particularly those that postulate that inversions achieve a selective advantage through the maintenance of co-adapted allele complexes.
Zdroje
1. SturtevantAH (1917) Genetic factors affecting the strength of linkage in Drosophila. Proc Natl Acad Sci U S A 3: 555–558.
2. NoorMAF, GramsKL, BertucciLA, ReilandJ (2001) Chromosomal inversions and the reproductive isolation of species. Proc Natl Acad Sci U S A 98: 12084–88.
3. RiesebergLH (2001) Chromosomal rearrangements and speciation. Trends Ecol. Evol 16: 351–58.
4. KirkpatrickM, BartonN (2006) Chromosome inversions, local adaptation and speciation. Genetics 173: 419–34.
5. SandlerL, HiraizumiY, SandlerI (1959) Meiotic drive in natural populations of Drosophila melanogaster. I. The cytogenetic basis of segregation distortion. Genetics 44: 233–250.
6. JaenikeJ (2001) Sex chromosome meiotic drive. Ann Rev Ecol System 32: 25–49.
7. PresgravesDC, GerardPR, CherukuriA, LyttleTW (2009) Large-scale selective sweep among segregation distorter chromosomes in African populations of Drosophila melanogaster. PLoS Genet 5: e1000463.
8. HoffmannAA, RiesebergLH (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.
9. White MJD (1973) Animal Cytology and Evolution, Third Ed. Cambridge University Press, London.
10. Krimbas CB, Powell JR (1992) Drosophila Inversion Polymorphism. CRC Press, Boca Raton, FL.
11. Sperlich D, Pfriem P (1986) Chromosomal polymorphism in natural and experimental populations. 257–309 in The Genetics and Biology of Drosophila. Eds. Ashburner M, Carson HL, Thomson JN. Academic Press, New York, NY.
12. StalkerHD (1976) Chromosome studies in wild populations of Drosophila melanogaster. Genetics 82: 323–347.
13. MettlerLE, VoelkerRA, MukaiT (1977) Inversion clines in populations of Drosophila melanogaster. Genetics 87: 169–176.
14. StalkerHD (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.
15. KnibbWR, OakenshotJG, GibsonJB (1981) Chromosome inversion polymorphism in Drosophila melanogaster.1. Latitudinal clines and associations between inversions in Australasian populations. Genetics 98: 833–847.
16. InoueY (1979) Seasonal changes of inversion frequencies of Drosophila melanogaster. Annual Report of the National Institute of Genetics (Japan) 29: 77.
17. WatanabeT (1969) Frequency of deleterious chromosomes and allelism between lethal genes in Japanese natural populations of Drosophila melanogaster. Japanese J Genet 44: 171–187.
18. WatanabeTK, WatanabeT (1973) Fertility genes in natural populations of Drosophila melanogaster. III. Superiority of inversion heterozygotes. Evolution 27: 468–475.
19. AndolfattoP, WallJD, KreitmanM (1999) Unusual haplotype structure at the proximal breakpoint of In(2L)t in a natural population of Drosophila melanogaster. Genetics 153: 1297–311.
20. MatzkinLM, MerrittTJS, ZhuCT, EanesWF (2005) The structure and population genetics of the breakpoints associated with the cosmopolitan chromosomal inversion In(3R)Payne in Drosophila melanogaster. Genetics 170: 1143–52.
21. WesleyCS, EanesWF (1994) Isolation and analysis of the breakpoint sequences of chromosome inversion In(3L)Payne in Drosophila melanogaster. Proc Natl Acad Sci U S A 91: 3132–3136.
22. HassonE, EanesWF (1996) Contrasting histories of three gene regions associated with In(3L)Payne of Drosophila melanogaster. Genetics 144: 1565–1575.
23. Corbett-DetigRB, CardenoC, LangleyCH (2012) Sequence-based detection and breakpoint assembly of polymorphic inversions. Genetics 192: 131–7.
24. AulardS, DavidJR, LemeunierF (2002) Chromosomal inversion polymorphism in Afrotropical populations of Drosophila melanogaster. Genet Res 79: 49–63.
25. PoolJE, Corbett-DetigRB, SuginoRP, StevensKA, CardenoCM, et al. (2012) Population genomics of sub-Saharan Drosophila melanogaster: African diversity and non-African admixture. Cosubmission
26. MackayTFC, RichardsS, StoneEA, BarbadillaA, AyrolesJF, et al. (2012) The Drosophila melanogaster genetic reference panel. Nature 482: 173–178.
27. LiH, StephanW (2006) Inferring the demographic history and rate of adaptive substitution in Drosophila. PLoS Genet 2: e166.
28. ThorntonKR, AndolfattoP (2006) Approximate Bayesian inference reveals evidence for a recent, severe bottleneck in a Netherlands population of Drosophila melanogaster. Genetics 172: 1607–1619.
29. GlinkaS, OmettoL, MoussetS, StephanW, De LorenzoD (2003) Demography and natural selection have shaped genetic variation in Drosophila melanogaster a multi-locus approach. Genetics 165: 1269–1278.
30. LiH, DurbinR (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 2078–2079.
31. LiH, HandsakerB, WysokerA, FennellT, RuanJ, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078–2079.
32. Maynard SmithJ, HaighJ (1974) The hitch-hiking effect of a favourable gene. Genet Res Camb 23: 23–35.
33. LangleyCH, StevensK, CardenoC, LeeYCG, SchriderDR, et al. (2012) Genomic variation in natural populations of Drosophila melanogaster. Genetics, revisions submitted
34. WallaceAG, DetweilerD, SchaefferSW (2011) Evolutionary History of the Third Chromosome Gene Arrangements of Drosophila pseudoobscura Inferred from Inversion Breakpoints. Mol Biol Evol 28(8): 2219–2229.
35. TajimaF (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585–595.
36. SchaefferSW (2002) Molecular population genetics of sequence length diversity in the Adh region of Drosophila pseudoobscura. Gen Res 80: 163–175.
37. PritchardJK, SeielstadMT, Perez-LezaunA, FeldmanMW (1999) Population growth of human Y chromosomes: a study of Y chromosome microsatellites. Mol Biol Evol 16: 1791–1798.
38. BeaumontMA, ZhangW, BaldingDJ (2002) Approximate Bayesian computation in population genetics. Genetics 162: 2025–2035.
39. NielsenR, WilliamsonS, KimY, HubiszMJ, ClarkAG, et al. (2005) Genomic scans for selective sweeps using SNP data. Genome Res 15: 1566–1575.
40. AndolfattoP, DepaulisF, NavarroA (2001) Inversion polymorphisms and nucleotide variability in Drosophila. Genet Res 77: 1–8.
41. AulardS, MontiL, ChaminadeN, LemeunierF (2004) Mitotic and polytene chromosomes: comparisons between Drosophila melanogaster and Drosophila simulans. Genetica 120: 137–150.
42. RanzJM, MaurinD, ChanYS, GrotthussMV, HillierLM, et al. (2007) Principles of genome evolution in the Drosophila melanogaster species group. PLoS Biol 5: 1366–1381.
43. PoolJE, AquadroCF (2006) History and structure of sub-Saharan populations of Drosophila melanogaster. Genetics 174: 915–929.
44. NavarroA, BetranE, BarbadillaA, RuizA (1997) Recombination and gene flux caused by gene conversion and crossing over in inversion heterokaryotypes. Genetics 146: 695–709.
45. PattersonN, PriceAL, ReichD (2006) Population structure and eigenanalysis. PLoS Genet 2(12): e190.
46. KulathinalRJ, StevisonLS, NoorMAF (2009) The genomics of speciation in Drosophila: diversity, divergence, and introgression estimated using low-coverage genome sequencing. PLoS Genet 5: e1000550.
47. PayneF (1924) Crossover modifiers in the third chromosome of Drosophila melanogaster. Genetics 9: 327–342.
48. NavarroA, BarbadillaA, RuizA (2000) Effect of inversion polymorphism on the neutral nucleotide variability of linked chromosomal regions in Drosophila. Genetics 155: 685–698.
49. BaudryE, ViginierB, VeuilleM (2004) Non-African populations of Drosophila melanogaster have a unique origin. Mol Biol Evol 21: 1482–1491.
50. Dobzhansky, T., 1951 Genetics and the Origin of Species, Ed. 3. Columbia University Press, New York.
51. Maynard SmithJ, HaighJ (1974) The hitch-hiking effect of a favourable gene. Genet Res 23: 23–35.
52. CharlesworthB (1994) The Effect of Background Selection Against Deleterious Mutations on Weakly Selected, Linked Variants. Genet. Res 63: 213–227.
53. RichardsS, LiuY, BettencourtBR, HradeckyP, LetovskyS, et al. (2005) Comparative genome sequencing of Drosophila pseudoobscura: Chromosomal, gene, and cis-element evolution. Genome Res 15: 1–18.
54. ReedFA, ReevesRG, AquadroCF (2005) Evidence of susceptibility and resistance to cryptic X-linked meiotic drive in natural populations of Drosophila melanogaster. Evolution 59: 1280–1291.
55. NovitskiE, HanksGD (1961) The analysis of irradiated Drosophila populations for instances of meiotic drive. Nature 190: 989–990.
56. HanksGD (1968) RD (Recovery Disrupter) activity associated with various wild-type X chromosomes. Dros Inf Ser 43: 98.
57. AdamsMD, CelnikerSE, HoltRA, EvansCA, GocayneJD, et al. (2000) The genome sequence of Drosophila melanogaster. Science 287: 2185–2195.
58. ThompsonJD, HigginsDG, GibsonTJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673–4680.
59. HuTT, EisenMB, ThorntonKR, AndolfattoP (2012) A second generation assembly of the Drosophila simulans genome provides new insights into patterns of lineage-specific divergence. Genome Res Published in Advance August 30. doi:10.1101/gr.141689.112.
60. HudsonRR (2002) Generating samples under a Wright-Fisher neutral model. Bioinformatics 18: 337–338.
61. HudsonRR, SlatkinM, MaddisonWP (1992) Estimation of levels of gene flow from DNA-sequence data. Genetics 132: 583–589.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 12
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
Najčítanejšie v tomto čísle
- Population Genomics of Sub-Saharan : African Diversity and Non-African Admixture
- Insertion/Deletion Polymorphisms in the Promoter Are a Risk Factor for Bladder Exstrophy Epispadias Complex
- Mi2β Is Required for γ-Globin Gene Silencing: Temporal Assembly of a GATA-1-FOG-1-Mi2 Repressor Complex in β-YAC Transgenic Mice
- Deciphering the Transcriptional-Regulatory Network of Flocculation in