Intrapopulation Genome Size Variation in Reflects Life History Variation and Plasticity

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Genome size evolution is ubiquitous, and–even after decades of research–mysterious. There are two major classes of hypotheses regarding genome size evolution, those that attribute its causes to evolutionarily neutral processes and those that suggest a role for selection. Numerous correlations between genome size and fitness-related phenotypes have been documented, suggesting selection could play a role in genome size evolution. Unfortunately, many of the effects in those studies are confounded with factors that could provide alternative explanations. Here, we show that 211 inbred strains of Drosophila melanogaster exhibit abundant variation in genome size, which correlates with life history traits in a temperature-dependent manner. Gene expression analyses suggest a role for differences in metabolism between strains with large and small genomes. Thus, there is genetic variation in genome size within D. melanogaster, and this variation is connected to variation in environmentally dependent life history traits. These observations indicate that selection is indeed a potential mechanism by which genome size can evolve. Our results also suggest that higher levels of genetic architecture may explain some of the genetic contribution to biologically important complex traits and raise the possibility that nucleotide quantity can contribute to phenotype in addition to quality.

Vyšlo v časopise: Intrapopulation Genome Size Variation in Reflects Life History Variation and Plasticity. PLoS Genet 10(7): e32767. doi:10.1371/journal.pgen.1004522
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004522

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Zdroje

1. AlvarezfusterA, JuanC, PetitpierreE (1991) Genome size in Tribolium flour beetles – interspecifc and intraspecific variation. Genet Res 58: 1–5.

2. MarescalchiO, ScaliV, ZuccottiM (1998) Flow-cytometric analyses of intraspecific genome size variations in Bacillus atticus (Insecta, Phasmatodea). Genome 41: 629–635.

3. NardonC, DeceliereG, LoevenbruckC, WeissM, VieiraC, et al. (2005) Is genome size influenced by colonization of new environments in dipteran species? Mol Ecol 14: 869–878.

4. SharafK, BuresP, HorovaL, PavlicekT, NevoE (2008) Distribution of abundance and genome size variability in the grain beetle Oryzaephilus surinamensis (Linnaeus, 1758) (Coleoptera: Silvanidae). Zool Middle East 45: 79–89.

5. SharafK, HorovaL, PavlicekT, NevoE, BuresP (2010) Genome size and base composition in Oryzaephilus surinamensis (Coleoptera: Sylvanidae) and differences between native (feral) and silo pest populations in Israel. J Stored Prod Res 46: 34–37.

6. SantuariL, HardtkeCS (2010) The case for resequencing studies of Arabidopsis thaliana accessions: mining the dark matter of natural genetic variation. F1000 Biol Rep 2: 85.

7. BiemontC (2008) Genome size evolution: within-species variation in genome size. Heredity (Edinb) 101: 297–298.

8. VieiraC, NardonC, ArpinC, LepetitD, BiemontC (2002) Evolution of genome size in Drosophila. Is the invader's genome being invaded by transposable elements? Mol Biol Evol 19: 1154–1161.

9. GregoryTR (2004) Insertion-deletion biases and the evolution of genome size. Gene 324: 15–34.

10. GregoryTR, JohnstonJS (2008) Genome size diversity in the family Drosophilidae. Heredity (Edinb) 101: 228–238.

11. MuellerRL, GregoryTR, GregorySM, HsiehA, BooreJL (2008) Genome size, cell size, and the evolution of enucleated erythrocytes in attenuate salamanders. Zoology (Jena) 111: 218–230.

12. PetrovD (1997) Slow but Steady: Reduction of genome size through biased mutation. Plant Cell 9: 1900–1901.

13. PetrovDA, SangsterTA, JohnstonJS, HartlDL, ShawKL (2000) Evidence for DNA loss as a determinant of genome size. Science 287: 1060–1062.

14. PetrovDA (2002) Mutational equilibrium model of genome size evolution. Theor Popul Biol 61: 531–544.

15. LynchM, ConeryJS (2003) The origins of genome complexity. Science 302: 1401–1404.

16. HessenDO, DaufresneM, LeinaasHP (2013) Temperature-size relations from the cellular-genomic perspective. Biol Rev Camb Philos Soc 88: 476–489.

17. Schmidt-OttU, RafiqiAM, SanderK, JohnstonJS (2009) Extremely small genomes in two unrelated dipteran insects with shared early developmental traits. Dev Genes Evol 219: 207–210.

18. BennettMD, LeitchIJ, HansonL (1998) DNA amounts in two samples of angiosperm weeds. Ann Bot 82: 121–134.

19. LynchM, BobayLM, CataniaF, GoutJF, RhoM (2011) The repatterning of eukaryotic genomes by random genetic drift. Annu Rev Genomics Hum Genet 12: 347–366.

20. BennettMD, PriceHJ, JohnstonJS (2008) Anthocyanin inhibits propidium iodide DNA fluorescence in Euphorbia pulcherrima: implications for genome size variation and flow cytometry. Ann Bot 101: 777–790.

21. AtkinsonD (1994) Temperature and organism size – a biological law for ectotherms. Adv Ecol Res 25: 1–58.

22. LuoLG, DingGH, JiX (2010) Income breeding and temperature-induced plasticity in reproductive traits in lizards. J Exp Biol 213: 2073–2078.

23. AzevedoRB, FrenchV, PartridgeL (2002) Temperature modulates epidermal cell size in Drosophila melanogaster. J Insect Physiol 48: 231–237.

24. HallasR, SchifferM, HoffmannAA (2002) Clinal variation in Drosophila serrata for stress resistance and body size. Genet Res 79: 141–148.

25. KolaczkowskiB, KernAD, HollowayAK, BegunDJ (2011) Genomic differentiation between temperate and tropical Australian populations of Drosophila melanogaster. Genetics 187: 245–260.

26. MayrE (1956) Geographical character gradients and climatic adaptation. Evolution 10: 105–108.

27. TrottaV, CalboliFC, ZiosiM, GuerraD, PezzoliMC, et al. (2006) Thermal plasticity in Drosophila melanogaster: a comparison of geographic populations. BMC Evol Biol 6: 67.

28. RobertsonFW (1966) The ecological genetics of growth in Drosophila. 8. Adaptation to a new diet. Genet Res 8: 165–179.

29. PartridgeL, LangelanR, FowlerK, ZwaanB, FrenchV (1999) Correlated responses to selection on body size in Drosophila melanogaster. Genet Res 74: 43–54.

30. PartridgeL, ProwseN, PignatelliP (1999) Another set of responses and correlated responses to selection on age at reproduction in Drosophila melanogaster. P Roy Soc B-Biol Sci 266: 255–261.

31. LongTAF, PischeddaA, NicholsRV, RiceWR (2010) The timing of mating influences reproductive success in Drosophila melanogaster: implications for sexual conflict. J Evol Biol 23: 1024–1032.

32. MackayTF, RichardsS, StoneEA, BarbadillaA, AyrolesJF, et al. (2012) The Drosophila melanogaster Genetic Reference Panel. Nature 482: 173–178.

33. HuangW, MassourasA, InoueY, PeifferJ, RàmiaM, et al. (2014) Natural variation in genome architecture among 205 Drosophila melanogaster Genetic Reference Panel lines. Genome Res doi:10.1101/gr.171546.113

34. BennettMD, LeitchIJ, PriceHJ, JohnstonJS (2003) Comparisons with Caenorhabditis (approximately 100 Mb) and Drosophila (approximately 175 Mb) using flow cytometry show genome size in Arabidopsis to be approximately 157 Mb and thus approximately 25% larger than the Arabidopsis genome initiative estimate of approximately 125 Mb. Ann Bot 91: 547–557.

35. GreilhuberJ (2005) Intraspecific variation in genome size in angiosperms: Identifiying its existence. Ann Bot (London) 95: 91–98.

36. JohnstonJS, SchoenerM, McMahonDP (2013) DNA underreplication in the majority of nuclei in the Drosophila melanogaster thorax: evidence from Suur and flow cytometry. J Mol Biol Res 3: 47.

37. AyrolesJF, CarboneMA, StoneEA, JordanKW, LymanRF, et al. (2009) Systems genetics of complex traits in Drosophila melanogaster. Nat Genet 41: 299–307.

38. BernsteinBE, DunhamI, KundajeA, AldredSF, CollinsPJ, et al. (2012) An integrated encyclopedia of DNA elements in the human genome. Nature 489: 57–74.

39. DobzhanskyT, SturtevantAH (1938) Inversions in the chromosomes of Drosophila pseudoobscura. Genetics 23: 28–64.

40. KnibbWR, OakeshottJG, GibsonJB (1981) Chromosome inversion polymorphisms in Drosophila melanogaster. I. Latitudinal clines and associations between inversions in Australasian populations. Genetics 98: 833–847.

41. Cyrus ChuCY, LeeRD (2012) Sexual dimorphism and sexual selection: a unified economic analysis. Theor Popul Biol 82: 355–363.

42. GhoshSM, JoshiA (2012) Evolution of reproductive isolation as a by-product of divergent life-history evolution in laboratory populations of Drosophila melanogaster. Ecol Evol 2: 3214–3226.

43. HanX, FuJ (2013) Does life history shape sexual size dimorphism in anurans? A comparative analysis. BMC Evol Biol 13: 27.

44. KotrschalA, RasanenK, KristjanssonBK, SennM, KolmN (2012) Extreme sexual brain size dimorphism in sticklebacks: a consequence of the cognitive challenges of sex and parenting? PLoS One 7: e30055.

45. AtwellS, HuangYS, VilhjalmssonBJ, WillemsG, HortonM, et al. (2010) Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465: 627–631.

46. KorteA, VilhjalmssonBJ, SeguraV, PlattA, LongQ, et al. (2012) A mixed-model approach for genome-wide association studies of correlated traits in structured populations. Nat Genet 44: 1066–1071.

47. HareEE, JohnstonJS (2011) Genome size determination using flow cytometry of propidium iodide-stained nuclei. Methods Mol Biol 772: 3–12.

48. CridlandJM, MacdonaldSJ, LongAD, ThorntonKR (2013) Abundance and distribution of transposable elements in two Drosophila QTL mapping resources. Mol Biol Evol 30: 2311–2327.

49. LiC, WongWH (2001) Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci U S A 98: 31–36.

50. BaldiP, LongAD (2001) A Bayesian framework for the analysis of microarray expression data: regularized t -test and statistical inferences of gene changes. Bioinformatics 17: 509–519.

51. StoreyJD, TibshiraniR (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci U S A 100: 9440–9445.

52. HuangDW, ShermanBT, LempickiRA (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37: 1–13.

53. HuangDW, ShermanBT, LempickiRA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44–57.

54. BoyleEI, WengS, GollubJ, JinH, BotsteinD, et al. (2004) GO::TermFinder–open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics 20: 3710–3715.