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Evolutionary Biology

, Volume 45, Issue 3, pp 248–258 | Cite as

Same-Sex Twin Pair Phenotypic Correlations are Consistent with Human Y Chromosome Promoting Phenotypic Heterogeneity

  • Carlos Díaz-Castillo
Synthesis Paper

Abstract

Junk DNA has been long appreciated as an evolutionary facilitator because it can participate in the causation of genetic variation such as chromosome rearrangements and can be exapted into coding or regulatory elements. Recently, it has been proposed that junk DNA variation within natural populations indirectly causes a phenotypic heterogeneity that subsequently promotes genetic capacitance, i.e., the random fluctuation of genetic variation. Junk DNA role as capacitor might drive population traits such as sexual dimorphism, spatiotemporal dynamics, or genetic diversification leading into speciation. Whether the human species also showed junk DNA-based capacitance manifested as a junk DNA-dependent phenotypic heterogeneity that contributed to the etiology and expression of diseases or the evolutionary history of human populations is intriguing. Because the human Y chromosome is highly enriched in junk DNA, humans are sexually dimorphic for the genomic content in junk DNA. Thus, it would be expected that junk DNA-based capacitance in humans were manifested as a sexual dimorphism for phenotypic heterogeneity. Here, I gather supporting evidence for the existence of a sexual dimorphism for putative junk DNA-based phenotypic heterogeneity by analyzing same-sex twin pairs phenotypic concordance.

Keywords

Junk DNA Evolutionary capacitance Twin studies Y chromosome Phenotypic heterogeneity Missing heritability 

Notes

Acknowledgements

The author wants to express his deepest gratitude to Raquel Chamorro-Garcia for valuable comments and constant support.

Compliance with Ethical Standards

Conflict of interest

The author declares that he has no conflict of interest.

Supplementary material

11692_2018_9454_MOESM1_ESM.xlsx (50 kb)
Supplementary material 1 (XLSX 49 KB)
11692_2018_9454_MOESM2_ESM.docx (28 kb)
Supplementary material 2 (DOCX 28 KB)

References

  1. Ackermann, M. (2015). A functional perspective on phenotypic heterogeneity in microorganisms. Nature Reviews Microbiology, 13(8), 497–508.  https://doi.org/10.1038/nrmicro3491.PubMedCrossRefGoogle Scholar
  2. Ahmad, K., & Henikoff, S. (2001). Modulation of a transcription factor counteracts heterochromatic gene silencing in Drosophila. Cell, 104(6), 839–847.PubMedCrossRefGoogle Scholar
  3. Allshire, R. C., & Madhani, H. D. (2018). Ten principles of heterochromatin formation and function. Nature Reviews Molecular Cell Biology, 19(4), 229–244.  https://doi.org/10.1038/nrm.2017.119.PubMedCrossRefGoogle Scholar
  4. Altschuler, S. J., & Wu, L. F. (2010). Cellular heterogeneity: Do differences make a difference? Cell, 141(4), 559–563.  https://doi.org/10.1016/j.cell.2010.04.033.PubMedPubMedCentralCrossRefGoogle Scholar
  5. Bachtrog, D. (2013). Y-chromosome evolution: Emerging insights into processes of Y-chromosome degeneration. Nature Reviews Genetics, 14(2), 113–124.  https://doi.org/10.1038/nrg3366.PubMedPubMedCentralCrossRefGoogle Scholar
  6. Banaszynski, L. A., Allis, C. D., & Lewis, P. W. (2010). Histone variants in metazoan development. Developmental Cell, 19(5), 662–674.  https://doi.org/10.1016/j.devcel.2010.10.014.PubMedPubMedCentralCrossRefGoogle Scholar
  7. Baroux, C., Autran, D., Gillmor, C. S., Grimanelli, D., & Grossniklaus, U. (2008). The maternal to zygotic transition in animals and plants. Cold Spring Harbor Symposia on Quantitative Biologyol, 73(0), 89–100.  https://doi.org/10.1101/sqb.2008.73.053.CrossRefGoogle Scholar
  8. Berloco, M., Palumbo, G., Piacentini, L., Pimpinelli, S., & Fanti, L. (2014). Position effect variegation and viability are both sensitive to dosage of constitutive heterochromatin in Drosophila. G3: Genes, Genomes, Genetics, 4(9), 1709–1716.  https://doi.org/10.1534/g3.114.013045.CrossRefGoogle Scholar
  9. Biemont, C. (2010). A brief history of the status of transposable elements: From junk DNA to major players in evolution. Genetics, 186(4), 1085–1093.  https://doi.org/10.1534/genetics.110.124180.PubMedPubMedCentralCrossRefGoogle Scholar
  10. Brown, E., & Bachtrog, D. (2017). The Drosophila Y chromosome affects heterochromatin integrity genome-wide. bioRxiv, 2017, 156000Google Scholar
  11. Case, L. K., & Teuscher, C. (2015). Y genetic variation and phenotypic diversity in health and disease. Biology of Sex Differences, 6, 6.  https://doi.org/10.1186/s13293-015-0024-z.PubMedPubMedCentralCrossRefGoogle Scholar
  12. Chamorro-Garcia, R., Díaz-Castillo, C., Shoucri, B. M., Kach, H., Leavitt, R., Shioda, T., & Blumberg, B. (2017). Ancestral perinatal obesogen exposure results in a transgenerational thrifty phenotype in mice. Nature Communications, 8(1), 2012.  https://doi.org/10.1038/s41467-017-01944-z.PubMedPubMedCentralCrossRefGoogle Scholar
  13. Cohen, S., Agmon, N., Yacobi, K., Mislovati, M., & Segal, D. (2005). Evidence for rolling circle replication of tandem genes in Drosophila. Nucleic Acids Research, 33(14), 4519–4526.  https://doi.org/10.1093/nar/gki764.PubMedPubMedCentralCrossRefGoogle Scholar
  14. Cohen, S., & Segal, D. (2009). Extrachromosomal circular DNA in eukaryotes: Possible involvement in the plasticity of tandem repeats. Cytogenetic and Genome Research, 124(3–4), 327–338.  https://doi.org/10.1159/000218136.PubMedCrossRefGoogle Scholar
  15. Díaz-Castillo, C. (2015). Evidence for a sexual dimorphism in gene expression noise in metazoan species. PeerJ, 3, e750.  https://doi.org/10.7717/peerj.750.PubMedPubMedCentralCrossRefGoogle Scholar
  16. Díaz-Castillo, C. (2017a). Junk DNA and genome evolution. eLS.  https://doi.org/10.1002/9780470015902.a0027509.CrossRefGoogle Scholar
  17. Díaz-Castillo, C. (2017b). Junk DNA contribution to evolutionary capacitance can drive species dynamics. Evolutionary Biology, 44(2), 190–205.  https://doi.org/10.1007/s11692-016-9404-5.CrossRefGoogle Scholar
  18. Díaz-Castillo, C. (2017c). Transcriptome dynamics along axolotl regenerative development are consistent with an extensive reduction in gene expression heterogeneity in dedifferentiated cells. PeerJ, 5, e4004.  https://doi.org/10.7717/peerj.4004.PubMedPubMedCentralCrossRefGoogle Scholar
  19. Dimitri, P., & Pisano, C. (1989). Position effect variegation in Drosophila melanogaster: Relationship between suppression effect and the amount of Y chromosome. Genetics, 122(4), 793–800.PubMedPubMedCentralGoogle Scholar
  20. Doolittle, W. F. (2013). Is junk DNA bunk? A critique of ENCODE. Proceedings of the National Academy of Sciences of the United States of America, 110(14), 5294–5300.  https://doi.org/10.1073/pnas.1221376110.PubMedPubMedCentralCrossRefGoogle Scholar
  21. Doolittle, W. F., Brunet, T. D., Linquist, S., & Gregory, T. R. (2014). Distinguishing between “function” and “effect” in genome biology. Genome Biology and Evolution, 6(5), 1234–1237.  https://doi.org/10.1093/gbe/evu098.PubMedPubMedCentralCrossRefGoogle Scholar
  22. Ehrenreich, I. M., & Pfennig, D. W. (2016). Genetic assimilation: A review of its potential proximate causes and evolutionary consequences. Annals of Botany, 117(5), 769–779.  https://doi.org/10.1093/aob/mcv130.PubMedCrossRefGoogle Scholar
  23. Elgin, S. C., & Reuter, G. (2013). Position-effect variegation, heterochromatin formation, and gene silencing in Drosophila. Cold Spring Harbor Perspectives in Biology, 5(8), a017780.  https://doi.org/10.1101/cshperspect.a017780.PubMedPubMedCentralCrossRefGoogle Scholar
  24. Elliott, T. A., & Gregory, T. R. (2015). What’s in a genome? The C-value enigma and the evolution of eukaryotic genome content. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 370(1678), 20140331.  https://doi.org/10.1098/rstb.2014.0331.PubMedPubMedCentralCrossRefGoogle Scholar
  25. Erdtmann, B. (1982). Aspects of evaluation, significance, and evolution of human C-band heteromorphism. Human Genetics, 61(4), 281–294.PubMedCrossRefGoogle Scholar
  26. Feinberg, A. P., & Irizarry, R. A. (2010). Evolution in health and medicine Sackler colloquium: Stochastic epigenetic variation as a driving force of development, evolutionary adaptation, and disease. Proceedings of the National Academy of Sciences of the United States of America, 107(Suppl 1), 1757–1764.  https://doi.org/10.1073/pnas.0906183107.PubMedCrossRefGoogle Scholar
  27. Flyamer, I. M., Gassler, J., Imakaev, M., Brandao, H. B., Ulianov, S. V., Abdennur, N.,... Tachibana-Konwalski, K. (2017). Single-nucleus Hi-C reveals unique chromatin reorganization at oocyte-to-zygote transition. Nature, 544(7648), 110–114.  https://doi.org/10.1038/nature21711.PubMedPubMedCentralCrossRefGoogle Scholar
  28. Forsman, A. (2015). Rethinking phenotypic plasticity and its consequences for individuals, populations and species. Heredity, 115(4), 276–284.  https://doi.org/10.1038/hdy.2014.92.PubMedCrossRefGoogle Scholar
  29. Francisco, F. O., & Lemos, B. (2014). How do y-chromosomes modulate genome-wide epigenetic states: Genome folding, chromatin sinks, and gene expression. Journal of Genomics, 2, 94–103.  https://doi.org/10.7150/jgen.8043.PubMedPubMedCentralCrossRefGoogle Scholar
  30. Freeling, M., Xu, J., Woodhouse, M., & Lisch, D. (2015). A solution to the C-value paradox and the function of junk DNA: The genome balance hypothesis. Molecular Plant, 8(6), 899–910.  https://doi.org/10.1016/j.molp.2015.02.009.PubMedCrossRefGoogle Scholar
  31. Gamperl, R., Ehmann, C., & Bachmann, K. (1982). Genome size and heterochromatin variation in rodents. Genetica, 58(3), 199–212.  https://doi.org/10.1007/bf00128014.CrossRefGoogle Scholar
  32. Gatti, M., & Pimpinelli, S. (1992). Functional elements in Drosophila melanogaster heterochromatin. Annual Review of Genetics, 26, 239–275.  https://doi.org/10.1146/annurev.ge.26.120192.001323.PubMedCrossRefGoogle Scholar
  33. Gemayel, R., Vinces, M. D., Legendre, M., & Verstrepen, K. J. (2010). Variable tandem repeats accelerate evolution of coding and regulatory sequences. Annual Review of Genetics, 44(1), 445–477.  https://doi.org/10.1146/annurev-genet-072610-155046.PubMedCrossRefGoogle Scholar
  34. Golic, K. G., Golic, M. M., & Pimpinelli, S. (1998). Imprinted control of gene activity in Drosophila. Current Biology, 8(23), 1273–1276.  https://doi.org/10.1016/S0960-9822(07)00537-4.PubMedCrossRefGoogle Scholar
  35. Graur, D. (2013). The origin of the term “junk DNA”: A historical whodunnit. Judge Starling. Retrieved from https://judgestarling.tumblr.com/post/64504735261/the-origin-of-the-term-junk-dna-a-historical.
  36. Graur, D. (2017). Rubbish DNA: The functionless fraction of the human genome. In Evolution of the Human Genome I (Vol. 500, pp. 19–60). Tokyo: SpringerCrossRefGoogle Scholar
  37. Graur, D. (2017). An upper limit on the functional fraction of the human genome. Genome Biology and Evolution, 9(7), 1880–1885.  https://doi.org/10.1093/gbe/evx121.PubMedPubMedCentralCrossRefGoogle Scholar
  38. Graur, D., Zheng, Y., & Azevedo, R. B. (2015). An evolutionary classification of genomic function. Genome Biology and Evolution, 7(3), 642–645.  https://doi.org/10.1093/gbe/evv021.PubMedPubMedCentralCrossRefGoogle Scholar
  39. Graur, D., Zheng, Y., Price, N., Azevedo, R. B., Zufall, R. A., & Elhaik, E. (2013). On the immortality of television sets: “Function” in the human genome according to the evolution-free gospel of ENCODE. Genome Biology and Evolution, 5(3), 578–590.  https://doi.org/10.1093/gbe/evt028.PubMedPubMedCentralCrossRefGoogle Scholar
  40. Halfer, C. (1981). Interstrain heterochromatin polymorphisms in Drosophila melanogaster. Chromosoma, 84(2), 195–206.  https://doi.org/10.1007/BF00399131.PubMedCrossRefGoogle Scholar
  41. Hughes, J. F., & Page, D. C. (2015). The biology and evolution of mammalian Y chromosomes. Annual Review of Genetics, 49, 507–527.  https://doi.org/10.1146/annurev-genet-112414-055311.PubMedCrossRefGoogle Scholar
  42. Hughes, J. F., & Rozen, S. (2012). Genomics and genetics of human and primate y chromosomes. Annual Review of Genomics and Human Genetics, 13(1), 83–108.  https://doi.org/10.1146/annurev-genom-090711-163855.PubMedCrossRefGoogle Scholar
  43. Ibraimov, A. I., Mirrakhimov, M. M., Axenrod, E. I., & Kurmanova, G. U. (1986). Human chromosomal polymorphism. IX. Further data on the possible selective value of chromosomal Q-heterochromatin material. Human Genetics, 73(2), 151–156.PubMedCrossRefGoogle Scholar
  44. Jobling, M. A., & Tyler-Smith, C. (2017). Human Y-chromosome variation in the genome-sequencing era. Nature Reviews Genetics, 18(8), 485–497.  https://doi.org/10.1038/nrg.2017.36.PubMedCrossRefGoogle Scholar
  45. Jurka, J., Kapitonov, V. V., Kohany, O., & Jurka, M. V. (2007). Repetitive sequences in complex genomes: Structure and evolution. Annual Review of Genomics and Human Genetics, 8(1), 241–259.  https://doi.org/10.1146/annurev.genom.8.080706.092416.PubMedCrossRefGoogle Scholar
  46. Kellis, M., Wold, B., Snyder, M. P., Bernstein, B. E., Kundaje, A., Marinov, G. K.,... Hardison, R. C. (2014). Defining functional DNA elements in the human genome. Proceedings of the National Academy of Sciences of the United States of America, 111(17), 6131–6138.  https://doi.org/10.1073/pnas.1318948111.PubMedPubMedCentralCrossRefGoogle Scholar
  47. Kelly, S. A., Panhuis, T. M., & Stoehr, A. M. (2012). Phenotypic plasticity: Molecular mechanisms and adaptive significance. Comprehensive Physiology, 2(2), 1417–1439.  https://doi.org/10.1002/cphy.c110008.PubMedCrossRefGoogle Scholar
  48. King, D. G., Soller, M., & Kashi, Y. (1997). Evolutionary tuning knobs. Endeavour, 21(1), 36–40.  https://doi.org/10.1016/s0160-9327(97)01005-3.CrossRefGoogle Scholar
  49. Komin, N., & Skupin, A. (2017). How to address cellular heterogeneity by distribution biology. Current Opinion in Systems Biology, 3, 154–160.  https://doi.org/10.1016/j.coisb.2017.05.010.CrossRefGoogle Scholar
  50. Koonin, E. V. (2016). Splendor and misery of adaptation, or the importance of neutral null for understanding evolution. BMC Biology, 14(1), 114.  https://doi.org/10.1186/s12915-016-0338-2.PubMedPubMedCentralCrossRefGoogle Scholar
  51. Koonin, E. V., & Wolf, Y. I. (2010). Constraints and plasticity in genome and molecular-phenome evolution. Nature Reviews Genetics, 11(7), 487–498.  https://doi.org/10.1038/nrg2810.PubMedPubMedCentralCrossRefGoogle Scholar
  52. Liu, J., Francois, J. M., & Capp, J. P. (2016). Use of noise in gene expression as an experimental parameter to test phenotypic effects. Yeast, 33(6), 209–216.  https://doi.org/10.1002/yea.3152.PubMedCrossRefGoogle Scholar
  53. Lyckegaard, E. M., & Clark, A. G. (1989). Ribosomal DNA and Stellate gene copy number variation on the Y chromosome of Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America, 86(6), 1944–1948.PubMedPubMedCentralCrossRefGoogle Scholar
  54. Lyckegaard, E. M., & Clark, A. G. (1991). Evolution of ribosomal RNA gene copy number on the sex chromosomes of Drosophila melanogaster. Molecular Biology and Evolution, 8(4), 458–474.PubMedGoogle Scholar
  55. Mackay, T. F. (2014). Epistasis and quantitative traits: Using model organisms to study gene-gene interactions. Nature Reviews Genetics, 15(1), 22–33.  https://doi.org/10.1038/nrg3627.PubMedCrossRefGoogle Scholar
  56. Maggert, K. A., & Golic, K. G. (2002). The Y chromosome of Drosophila melanogaster exhibits chromosome-wide imprinting. Genetics, 162(3), 1245–1258.PubMedPubMedCentralGoogle Scholar
  57. Mank, J. E. (2012). Small but mighty: The evolutionary dynamics of W and Y sex chromosomes. Chromosome Research, 20(1), 21–33.  https://doi.org/10.1007/s10577-011-9251-2.PubMedPubMedCentralCrossRefGoogle Scholar
  58. Masel, J. (2013). Q&A: Evolutionary capacitance. BMC Biology, 11(1), 103.  https://doi.org/10.1186/1741-7007-11-103.PubMedPubMedCentralCrossRefGoogle Scholar
  59. Masel, J., & Trotter, M. V. (2010). Robustness and evolvability. Trends in Genetics, 26(9), 406–414.  https://doi.org/10.1016/j.tig.2010.06.002.PubMedCrossRefGoogle Scholar
  60. Massaia, A., & Xue, Y. (2017). Human Y chromosome copy number variation in the next generation sequencing era and beyond. Human Genetics, 136(5), 591–603.  https://doi.org/10.1007/s00439-017-1788-5.PubMedPubMedCentralCrossRefGoogle Scholar
  61. McCracken, A. A., Daly, P. A., Zolnick, M. R., & Clark, A. M. (1978). Twins and Q-banded chromosome polymorphisms. Human Genetics, 45(3), 253–258.PubMedCrossRefGoogle Scholar
  62. Michel, A. H., Kornmann, B., Dubrana, K., & Shore, D. (2005). Spontaneous rDNA copy number variation modulates Sir2 levels and epigenetic gene silencing. Genes & Development, 19(10), 1199–1210.  https://doi.org/10.1101/gad.340205.CrossRefGoogle Scholar
  63. Miklos, G. L., & John, B. (1979). Heterochromatin and satellite DNA in man: Properties and prospects. American Journal of Human Genetics, 31(3), 264–280.PubMedPubMedCentralGoogle Scholar
  64. Muller, H. J. (1930). Types of visible variations induced by X-rays in Drosophila. Journal of Genetics, 22(3), 299–334.  https://doi.org/10.1007/Bf02984195.CrossRefGoogle Scholar
  65. Niu, D. K., & Jiang, L. (2013). Can ENCODE tell us how much junk DNA we carry in our genome? Biochemical and Biophysical Research Communications, 430(4), 1340–1343.  https://doi.org/10.1016/j.bbrc.2012.12.074.PubMedCrossRefGoogle Scholar
  66. Nonaka, E., Svanback, R., Thibert-Plante, X., Englund, G., & Brannstrom, A. (2015). Mechanisms by which phenotypic plasticity affects adaptive divergence and ecological speciation. The American Naturalist, 186(5), E126–E143.  https://doi.org/10.1086/683231.CrossRefGoogle Scholar
  67. Nova, P., Reutter, B. A., Rabova, M., & Zima, J. (2002). Sex-chromosome heterochromatin variation in the wood mouse, Apodemus sylvaticus. Cytogenetic and Genome Research, 96(1–4), 186–190.PubMedCrossRefGoogle Scholar
  68. O’Meally, D., Patel, H. R., Stiglec, R., Sarre, S. D., Georges, A., Marshall Graves, J. A., & Ezaz, T. (2010). Non-homologous sex chromosomes of birds and snakes share repetitive sequences. Chromosome Research, 18(7), 787–800.  https://doi.org/10.1007/s10577-010-9152-9.PubMedCrossRefGoogle Scholar
  69. Ohno, S. (1972). So much “junk” DNA in our genome. Brookhaven Symposia in Biology, 23, 366–370.PubMedGoogle Scholar
  70. Oliver, K. R., & Greene, W. K. (2009). Transposable elements: Powerful facilitators of evolution. Bioessays, 31(7), 703–714.  https://doi.org/10.1002/bies.200800219.PubMedCrossRefGoogle Scholar
  71. Paaby, A. B., & Rockman, M. V. (2014). Cryptic genetic variation: Evolution’s hidden substrate. Nature Reviews Genetics, 15(4), 247–258.  https://doi.org/10.1038/nrg3688.PubMedPubMedCentralCrossRefGoogle Scholar
  72. Palazzo, A. F., & Gregory, T. R. (2014). The case for junk DNA. PLoS Genetics, 10(5), e1004351.  https://doi.org/10.1371/journal.pgen.1004351.PubMedPubMedCentralCrossRefGoogle Scholar
  73. Paredes, S., Branco, A. T., Hartl, D. L., Maggert, K. A., & Lemos, B. (2011). Ribosomal DNA deletions modulate genome-wide gene expression: “rDNA-sensitive” genes and natural variation. PLoS Genetics, 7(4), e1001376.  https://doi.org/10.1371/journal.pgen.1001376.PubMedPubMedCentralCrossRefGoogle Scholar
  74. Passarge, E. (1979). Emil Heitz and the concept of heterochromatin: Longitudinal chromosome differentiation was recognized fifty years ago. American Journal of Human Genetics, 31(2), 106–115.PubMedPubMedCentralGoogle Scholar
  75. Pedrosa, M. P., Salzano, F. M., Mattevi, M. S., & Viegas, J. (1983). Quantitative analysis of C-bands in chromosomes 1, 9, 16, and Y of twins. Acta Geneticae Medicae et Gemellologiae: Twin Research, 32(3–4), 257–260.PubMedCrossRefGoogle Scholar
  76. Pennisi, E. (2012). Genomics. ENCODE project writes eulogy for junk DNA. Science, 337(6099), 1159–1161.  https://doi.org/10.1126/science.337.6099.1159.PubMedCrossRefGoogle Scholar
  77. Phillippy, A. M. (2017). New advances in sequence assembly. Genome Research, 27(5), xi–xiii.  https://doi.org/10.1101/gr.223057.117.CrossRefGoogle Scholar
  78. Pigliucci, M. (2010). Genotype-phenotype mapping and the end of the ‘genes as blueprint’ metaphor. Philosophical Transactions of the Royal Society B: Biological Sciences, 365(1540), 557–566.  https://doi.org/10.1098/rstb.2009.0241.CrossRefGoogle Scholar
  79. Polderman, T. J., Benyamin, B., de Leeuw, C. A., Sullivan, P. F., van Bochoven, A., Visscher, P. M., & Posthuma, D. (2015). Meta-analysis of the heritability of human traits based on fifty years of twin studies. Nature Genetics, 47(7), 702–709.  https://doi.org/10.1038/ng.3285.PubMedCrossRefGoogle Scholar
  80. Poznik, G. D., Xue, Y., Mendez, F. L., Willems, T. F., Massaia, A., Wilson Sayres, M. A.,... Tyler-Smith, C. (2016). Punctuated bursts in human male demography inferred from 1,244 worldwide Y-chromosome sequences. Nature Genetics, 48(6), 593–599.  https://doi.org/10.1038/ng.3559.PubMedPubMedCentralCrossRefGoogle Scholar
  81. Prokop, J. W., & Deschepper, C. F. (2015). Chromosome Y genetic variants: Impact in animal models and on human disease. Physiological Genomics, 47(11), 525–537.  https://doi.org/10.1152/physiolgenomics.00074.2015.PubMedPubMedCentralCrossRefGoogle Scholar
  82. Rands, C. M., Meader, S., Ponting, C. P., & Lunter, G. (2014). 8.2% of the Human genome is constrained: Variation in rates of turnover across functional element classes in the human lineage. PLoS Genetics, 10(7), e1004525.  https://doi.org/10.1371/journal.pgen.1004525.PubMedPubMedCentralCrossRefGoogle Scholar
  83. Raser, J. M., & O’Shea, E. K. (2005). Noise in gene expression: Origins, consequences, and control. Science, 309(5743), 2010–2013.  https://doi.org/10.1126/science.1105891.PubMedPubMedCentralCrossRefGoogle Scholar
  84. Repping, S., van Daalen, S. K., Brown, L. G., Korver, C. M., Lange, J., Marszalek, J. D.,... Rozen, S. (2006). High mutation rates have driven extensive structural polymorphism among human Y chromosomes. Nature Genetics, 38(4), 463–467.  https://doi.org/10.1038/ng1754.PubMedCrossRefGoogle Scholar
  85. Rivas, G., & Minton, A. P. (2016). Macromolecular crowding in vitro, in vivo, and in between. Trends in Biochemical Sciences, 41(11), 970–981.  https://doi.org/10.1016/j.tibs.2016.08.013.PubMedPubMedCentralCrossRefGoogle Scholar
  86. Robin, J. D., & Magdinier, F. (2017). Higher-order chromatin organization in diseases: From chromosomal position effect to phenotype variegation. In Handbook of epigenetics: The new molecular and medical genetics, 2nd edn, New York: Elsevier, pp. 73–92.  https://doi.org/10.1016/B978-0-12-805388-1.00006-7.CrossRefGoogle Scholar
  87. Rutherford, S. L., & Lindquist, S. (1998). Hsp90 as a capacitor for morphological evolution. Nature, 396(6709), 336–342.  https://doi.org/10.1038/24550.PubMedCrossRefGoogle Scholar
  88. Sackton, T. B., & Hartl, D. L. (2016). Genotypic context and epistasis in individuals and populations. Cell, 166(2), 279–287.  https://doi.org/10.1016/j.cell.2016.06.047.PubMedPubMedCentralCrossRefGoogle Scholar
  89. Sahara, K., Yoshido, A., & Traut, W. (2012). Sex chromosome evolution in moths and butterflies. Chromosome Research, 20(1), 83–94.  https://doi.org/10.1007/s10577-011-9262-z.PubMedCrossRefGoogle Scholar
  90. Schlichting, C. D., & Wund, M. A. (2014). Phenotypic plasticity and epigenetic marking: An assessment of evidence for genetic accommodation. Evolution, 68(3), 656–672.  https://doi.org/10.1111/evo.12348.PubMedCrossRefGoogle Scholar
  91. Singh, L., Purdom, I. F., & Jones, K. W. (1980). Sex chromosome associated satellite DNA: Evolution and conservation. Chromosoma, 79(2), 137–157.PubMedCrossRefGoogle Scholar
  92. Strom, A. R., Emelyanov, A. V., Mir, M., Fyodorov, D. V., Darzacq, X., & Karpen, G. H. (2017). Phase separation drives heterochromatin domain formation. Nature, 547(7662), 241–245.  https://doi.org/10.1038/nature22989.PubMedPubMedCentralCrossRefGoogle Scholar
  93. Symmons, O., & Raj, A. (2016). What’s luck got to do with it: Single cells, multiple fates, and biological nondeterminism. Molecular Cell, 62(5), 788–802.  https://doi.org/10.1016/j.molcel.2016.05.023.PubMedPubMedCentralCrossRefGoogle Scholar
  94. Tadros, W., & Lipshitz, H. D. (2009). The maternal-to-zygotic transition: A play in two acts. Development, 136(18), 3033–3042.  https://doi.org/10.1242/dev.033183.PubMedCrossRefGoogle Scholar
  95. The Encode Project Consortium. (2012). An integrated encyclopedia of DNA elements in the human genome. Nature, 489(7414), 57–74.PubMedCentralCrossRefGoogle Scholar
  96. Timms, R. T., Tchasovnikarova, I. A., & Lehner, P. J. (2016). Position-effect variegation revisited: HUSHing up heterochromatin in human cells. Bioessays, 38(4), 333–343.  https://doi.org/10.1002/bies.201500184.PubMedCrossRefGoogle Scholar
  97. Tomaszkiewicz, M., Medvedev, P., & Makova, K. D. (2017). Y and W chromosome assemblies: Approaches and discoveries. Trends in Genetics, 33(4), 266–282.  https://doi.org/10.1016/j.tig.2017.01.008.PubMedCrossRefGoogle Scholar
  98. Van Dyke, D. L., Palmer, C. G., Nance, W. E., & Yu, P. L. (1977). Chromosome polymorphism and twin zygosity. American Journal of Human Genetics, 29(5), 431–447.PubMedPubMedCentralGoogle Scholar
  99. Viegas, J., & Salzano, F. M. (1978). C-bands in chromosomes 1,9, and 16 of twins. Human Genetics, 45(2), 127–130.PubMedCrossRefGoogle Scholar
  100. Voskarides, K. (2017). Y chromosome and cardiovascular risk: What are we missing? Atherosclerosis, 259, 97–98.  https://doi.org/10.1016/j.atherosclerosis.2017.02.026.PubMedCrossRefGoogle Scholar
  101. Waddington, C. H. (1953). Genetic assimilation of an acquired character. Evolution, 7(2), 118–126.  https://doi.org/10.2307/2405747.CrossRefGoogle Scholar
  102. Waddington, C. H. (1956). Genetic assimilation of the bithorax phenotype. Evolution, 10(1), 1–13.  https://doi.org/10.2307/2406091.CrossRefGoogle Scholar
  103. Yadav, S. K., Kumari, A., Javed, S., & Ali, S. (2014). DYZ1 arrays show sequence variation between the monozygotic males. BMC Genetics, 15, 19.  https://doi.org/10.1186/1471-2156-15-19.PubMedPubMedCentralCrossRefGoogle Scholar
  104. Yanagida, H., Gispan, A., Kadouri, N., Rozen, S., Sharon, M., Barkai, N., & Tawfik, D. S. (2015). The evolutionary potential of phenotypic mutations. PLoS Genetics, 11(8), e1005445.  https://doi.org/10.1371/journal.pgen.1005445.PubMedPubMedCentralCrossRefGoogle Scholar
  105. Yun, A. J., Lee, P. Y., & Doux, J. D. (2006). Efficient inefficiency: Biochemical “junk” may represent molecular bridesmaids awaiting emergent function as a buffer against environmental fluctuation. Medical Hypotheses, 67(4), 914–921.  https://doi.org/10.1016/j.mehy.2006.02.022.PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.IrvineUSA

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