Abstract
Because genomes are products of natural processes rather than “intelligent design,” all genomes contain functional and nonfunctional parts. The fraction of the genome that has no biological function is called “rubbish DNA.” Rubbish DNA consists of “junk DNA,” i.e., the fraction of the genome on which selection does not operate, and “garbage DNA,” i.e., sequences that lower the fitness of the organism but exist in the genome because purifying selection is neither omnipotent nor instantaneous. In this chapter, I (1) review the concepts of genomic function and functionlessness from an evolutionary perspective, (2) present a precise nomenclature of genomic function, (3) discuss the evidence for the existence of vast quantities of junk DNA within the human genome, (4) discuss the mutational mechanisms responsible for generating junk DNA, (5) spell out the necessary evolutionary conditions for maintaining junk DNA, (6) outline various methodologies for estimating the functional fraction within the genome, and (7) present a recent estimate for the functional fraction of our genome.
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References
Adey A et al (2013) The haplotype-resolved genome and epigenome of the aneuploid HeLa cancer cell line. Nature 500:207–211
Ahituv N, Zhu Y, Visel A, Holt A, Afzal V, Pennacchio LA, Rubin EM (2007) Deletion of ultraconserved elements yields viable mice. PLoS Biol 5:e234
Amundson R, Lauder GV (1994) Function without purpose. Biol Philos 9:443–469
Andrés AM et al (2009) Targets of balancing selection in the human genome. Mol Biol Evol 26:2755–2764
Aparicio S et al (2002) Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 297:1301–1310
Aronson AI et al (1960) Biophysics. In: Year book 59: Carnegie Institution of Washington. Lord Baltimore Press, Baltimore, pp 229–289
Avarello R, Pedicini A, Caiulo A, Zuffardi O, Fraccaro M (1992) Evidence for an ancestral alphoid domain on the long arm of human chromosome 2. Hum Genet 89:247–249
Babushok DV et al (2007) A novel testis ubiquitin-binding protein gene arose by exon shuffling in hominoids. Genome Res 17:1129–1138
Bailey JA, Liu G, Eichler EE (2003) An Alu transposition model for the origin and expansion of human segmental duplications. Am J Hum Genet 73:823–834
Bartolomé C, Bello X, Maside X (2009) Widespread evidence for horizontal transfer of transposable elements across Drosophila genomes. Genome Biol 10:R22
Biémont C, Vieira C (2006) Junk DNA as an evolutionary force. Nature 443:521–524
Brenner S (1998) Refuge of spandrels. Curr Biol 8:R669
Britten RJ (1994) Evidence that most Alu sequences were inserted in a process that ceased about 30 million years ago. Proc Natl Acad Sci U S A 91:6148–6150
Brookfield JF (2000) Genomic sequencing: the complexity conundrum. Curr Biol 10:R514–R515
Brookfield JFY, Badge RM (1997) Population genetics models of transposable elements. Genetica 100:281–294
Brosius J, Gould SJ (1992) On “genomenclature”: a comprehensive (and respectful) taxonomy for pseudogenes and other “junk DNA”. Proc Natl Acad Sci U S A 89:10706–10710
Brunet TDP, Doolittle WF (2014) Getting “function” right. Proc Natl Acad Sci U S A 111:E3365
Burgess J (1985) An introduction to plant cell development. Cambridge University Press, Cambridge
Carlson CS, Thomas DJ, Eberle MA, Swanson JE, Livingston RJ, Rieder MJ, Nickerson DA (2005) Genomic regions exhibiting positive selection identified from dense genotype data. Genome Res 15:1553–1565
Cavalier-Smith T (1978) Nuclear volume control by nucleoskeletal DNA, selection for cell volume and cell growth rate, and the solution of the DNA C-value paradox. J Cell Sci 34:247–278
Cavalier-Smith T (1982) Skeletal DNA and the evolution of genome size. Annu Rev Biophys Bioeng 11:273–302
Cavalier-Smith T (ed) (1985) The evolution of genome size. Wiley, New York
Cavalier-Smith T (2005) Economy, speed and size matter: evolutionary forces driving nuclear genome miniaturization and expansion. Ann Bot 95:147–175
Chalopin D, Naville M, Plard F, Galiana D, Volff JN (2015) Comparative analysis of transposable elements highlights mobilome diversity and evolution in vertebrates. Genome Biol Evol 7:567–580
Chen YH et al (2003) KCNQ1 gain-of-function mutation in familial atrial fibrillation. Science 299:251–254
Chénais B, Caruso A, Hiard S, Casse N (2012) The impact of transposable elements on eukaryotic genomes: from genome size increase to genetic adaptation to stressful environments. Gene 509:7–15
Cho JH, Brant SR (2011) Recent insights into the genetics of inflammatory bowel disease. Gastroenterology 140:1704–1712
Chun S, Fay JC (2009) Identification of deleterious mutations within three human genomes. Genome Res 19:1553–1561
Comings DE (1972) The structure and function of chromatin. Adv Hum Genet 3:237–431
Conrad DF et al (2011) Variation in genome-wide mutation rates within and between human families. Nat Genet 43:712–714
Cooper GM, Shendure J (2011) Needles in stacks of needles: finding disease-causal. Nat Rev Genet 12:628–640
Cummins R (1975) Functional analysis. J Philos 72:741–765
Daniels SB, Peterson KR, Strausbaugh LD, Kidwell MG, Chovnick A (1990) Evidence for horizontal transmission of the P transposable element between Drosophila species. Genetics 124:339–355
Darlington CD (1937) Recent advances in cytology, 2nd edn. Blakiston, Philadelphia
De Gobbi M et al (2006) A regulatory SNP causes a human genetic disease by creating a new transcriptional promoter. Science 312:1215–1217
Denoeud F et al (2007) Prominent use of distal 5′ transcription start sites and discovery of a large number of additional exons in ENCODE regions. Genome Res 17:746–759
Dietrich FS et al (2004) The Ashbya gossypii genome as a tool for mapping the ancient Saccharomyces cerevisiae genome. Science 304:304–307
Doolittle WF (2013) Is junk DNA bunk? A critique of ENCODE. Proc Natl Acad Sci U S A 110:5294–5300
Doolittle WF, Sapienza C (1980) Selfish genes, the phenotype paradigm and genome evolution. Nature 284:601–603
Doolittle WF, Brunet TDP, Linquist S, Gregory TR (2014) Distinguishing between “function” and “effect” in genome biology. Genome Biol Evol 6:1234–1237
Douglas S et al (2001) The highly reduced genome of an enslaved algal nucleus. Nature 410:1091–1096
Eddy SR (2012) The C-value paradox, junk DNA and ENCODE. Curr Biol 22:R898–R899
Ehret CF, de Haller G (1963) Origin, development, and maturation of organelles and organelle systems of the cell surface in Paramecium. J Ultrastruct Res 23(Supplement 6):1–42
ENCODE Project Consortium (2012) An integrated encyclopedia of DNA elements in the human genome. Nature 489:57–74
Excoffier L, Hofer T, Foll M (2009) Detecting loci under selection in a hierarchically structured population. Heredity 103:285–298
Ezkurdia I et al (2014) Multiple evidence strands suggest that there may be as few as 19,000 human protein-coding genes. Hum Mol Genet 23:5866–5878
Faulkner GJ et al (2009) The regulated retrotransposon transcriptome of mammalian cells. Nat Genet 41:563–571
Fu W et al (2013) Analysis of 6,515 exomes reveals the recent origin of most human protein-coding variants. Nature 493:216–220
Gherman A et al (2007) Population bottlenecks as a potential major shaping force of human genome architecture. PLoS Genet 3:e119
Gilson PR, Su V, Slamovits CH, Reith ME, Keeling PJ, McFadden GI (2006) Complete nucleotide sequence of the chlorarachniophyte nucleomorph: nature’s smallest nucleus. Proc Natl Acad Sci U S A 103:9566–9571
Goldberg WM (2013) The biology of reefs and reef organisms. University of Chicago Press, Chicago
Graur D (2016) Molecular and genome evolution. Sinauer Associates, Sunderland
Graur D (2017) An upper limit on the functional fraction of the human genome. Genome Biol Evol 9:1880–1885
Graur D, Zheng Y, Price N, Azevedo RB, Zufall RA, Elhaik E (2013) On the immortality of television sets: “function” in the human genome according to the evolution-free gospel of ENCODE. Genome Biol Evol 5:578–590
Graur D, Zheng Y, Azevedo RB (2015) An evolutionary classification of genomic function. Genome Biol Evol 7:642–645
Gregory TR (2001) Coincidence, coevolution, or causation? DNA content, cell size, and the C-value enigma. Biol Rev 76:65–101
Gregory TR (2003) Variation across amphibian species in the size of the nuclear genome supports a pluralistic, hierarchical approach to the C-value enigma. Biol J Linn Soc 79:329–339
Greilhuber J, Leitch IJ (2013) Genome size and the phenotype. In: Leitch IJ, Greilhuber J, Dolezel J, Wendel J (eds) Plant genome diversity, vol 2. Springer, Wien, pp 323–344
Greilhuber J, Dolezel J, Lysák MA, Bennett MD (2005) The origin, evolution and proposed stabilization of the terms ‘genome size’ and ‘C-value’ to describe nuclear DNA contents. Ann Bot 95:255–260
Greilhuber J, Borsch T, Müller K, Worberg A, Porembski S, Barthlott W (2006) Smallest angiosperm genomes found in Lentibulariaceae, with chromosomes of bacterial size. Plant Biol 8:770–777
Grossman SR et al (2010) A composite of multiple signals distinguishes causal variants in regions of positive selection. Science 327:883–886
Grossman SR et al (2013) Identifying recent adaptations in large-scale genomic data. Cell 152:703–713
Haldane JBS (1937) The effect of variation on fitness. Am Nat 71:337–349
Hanson L, Brown RL, Boyd A, Johnson MA, Bennett MD (2003) First nuclear DNA C-values for 28 angiosperm genera. Ann Bot 91:31–38
Hare MP, Palumbi SR (2003) High intron sequence conservation across three mammalian orders suggests functional constraints. Mol Biol Evol 20:969–978
Hartl DL, Lohe AR, Lozovskaya ER (1997) Modern thoughts on an ancyent marinere: function, evolution, regulation. Annu Rev Genet 31:337–358
Hawkins JS, Kim H, Nason JD, Wing RA, Wendel JF (2006) Differential lineage-specific amplification of transposable elements is responsible for genome size variation in Gossypium. Genome Res 16:1252–1261
Hayden EC (2010) Life is complicated. Nature 464:664–667
Hazkani-Covo E, Zeller RM, Martin W (2010) Molecular poltergeists: mitochondrial DNA copies (numts) in sequenced nuclear genomes. PLoS Genet 6:e1000834
Hirose T, Shu MD, Steitz JA (2003) Splicing-dependent and –independent modes of assembly for intron-encoded box C/D snoRNPs in mammalian cells. Mol Cell 12:113–123
Huneman P (ed) (2013) Functions: selection and mechanisms. Springer, Dordrecht
Hurst LD (2013) Open questions: a logic (or lack thereof) of genome organization. BMC Biol 11:58
Ibarra-Laclette E et al (2013) Architecture and evolution of a minute plant genome. Nature 498:94–98
International Human Genome Sequencing Consortium (2004) Finishing the euchromatic sequence of the human genome. Nature 431:931–945
Jorgensen P, Edgington NP, Schneider BL, Rupes I, Tyers M, Futcher B (2007) The size of the nucleus increases as yeast cells grow. Mol Biol Cell 18:3523–3532
Kandouz M, Bier A, Carystinos GD, Alaoui-Jamali MA, Batist G (2004) Connexin43 pseudogene is expressed in tumor cells and inhibits growth. Oncogene 23:4763–4770
Kaufman SA (1971) Gene regulation networks: a theory for their global structures and behaviours. In: Moscona AA, Monroy A (eds) Current topics in developmental biology. Academic, New York, pp 145–182
Kauffman SA (1993) The origins of order: self-organization and selection in evolution. Oxford University Press, Oxford
Keightley PD, Eyre-Walker A (2000) Deleterious mutations and the evolution of sex. Science 209:331–333
Kelley JL et al (2014) Compact genome of the Antarctic midge is likely an adaptation to an extreme environment. Nat Commun 5:4611
Kellis M et al (2014) Defining functional DNA elements in the human genome. Proc Natl Acad Sci U S A 111:6131–6138
Kidwell MG (1992) Horizontal transfer of P-elements and other short inverted repeat transposons. Genetica 86:275–286
Kidwell MG (2002) Transposable elements and the evolution of genome size in eukaryotes. Genetica 115:49–63
Kimura M (1961) Some calculations on the mutational load. Jap J Genet 36:S179–S190
Kimura M, Maruyama T (1966) The mutational load with interactions in fitness. Genetics 54:1337–1351
Klotzko AJ (ed) (2001) The cloning sourcebook. Oxford University Press, Oxford
Kolata G (2010) Reanimated ‘junk’ DNA is found to cause disease. New York Times http://www.nytimes.com/2010/08/20/science/20gene.html?_r=0
Kong A et al (2012) Rate of de novo mutations and the importance of father’s age to disease risk. Nature 488:471–475
de Koning AP, Gu W, Castoe TA, Batzer MA, Pollock DD (2011) Repetitive elements may comprise over two-thirds of the human genome. PLoS Genet 7:e1002384
Kovach A et al (2010) The Pinus taeda genome is characterized by diverse and highly diverged repetitive sequences. BMC Genomics 11:420
Krams SM, Bromberg JS (2013) ENCODE: life, the universe and everything. Am J Transplant 13:245
Lander ES et al (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921
Lawrie DS, Petrov DA (2014) Comparative population genomics: power and principles for the inference of functionality. Trends Genet 30:133–139
Le Rouzic A, Boutin TS, Capy P (2007) Long-term evolution of transposable elements. Proc Nat Acad Sci 104:19375–19380
Levin HL, Moran JV (2011) Dynamic interactions between transposable elements and their hosts. Nature Rev Genet 12:615–627
Levy DL, Heald R (2010) Nuclear size is regulated by importin α and Ntf2 in Xenopus. Cell 143:288–298
Li H, Stephan W (2006) Inferring the demographic history and rate of adaptive substitution in Drosophila. PLoS Genet 2:e166
Li X et al (2011) Chromosome size in diploid eukaryotic species centers on the average length with a conserved boundary. Mol Biol Evol 28:1901–1911
Lloyd S (2001) Measures of complexity: a nonexhaustive list. IEEE Control Syst Mag 21(4):7–8
Lockton S, Ross-Ibarra J, Gaut BS (2008) Demography and weak selection drive patterns of transposable element diversity in natural populations of Arabidopsis lyrata. Proc Natl Acad Sci U S A 105:13965–13970
Lynch M (2006) The origins of eukaryotic gene structure. Mol Biol Evol 23:450–468
Lynch M (2010) Evolution of the mutation rate. Trends Genet 26:345–352
Lynch M, Conery JS (2003) The origins of genome complexity. Science 302:1401–1404
Lynch M, Bobay L-M, Catania F, Gout J-F, Rho M (2011) The repatterning of eukaryotic genomes by random genetic drift. Annu Rev Genomics Hum Genet 12:347–366
Makalowski W (2003) Not junk after all. Science 300:1246–1247
Marshall WF et al (2012) What determines cell size? BMC Biol 10:101
Maruyama T (1974) The age of a rare mutant gene in a large population. Am J Hum Genet 26:669–673
Massingham T, Goldman N (2005) Detecting amino acid sites under positive selection and purifying selection. Genetics 169:1753–1762
Mehta G, Jalan R, Mookerjee RP (2013) Cracking the ENCODE: from transcription to therapeutics. Hepatology 57:2532–2535
Millikan RG (1989) In defense of proper functions. Philos Sci 56:288–302
Mirsky AE, Ris H (1951) The desoxyribonucleic acid content of animal cells and its evolutionary significance. J Gen Physiol 34:451–462
Moran LA (2007) The deflated ego problem. http://sandwalk.blogspot.com/2007/05/deflated-ego-problem.html
Muller HJ (1950) Our load of mutations. Am J Hum Genet 2:111–176
Neander K (1991) Functions as selected effects: the conceptual analyst’s defense. Philos Sci 58:168–184
Nei M (2013) Mutation driven evolution. Oxford University Press, Oxford
Nelson DR (2004) “Frankenstein genes,” or the Mad Magazine version of the human pseudogenome. Hum Genomics 1:310–316
Neumann FR, Nurse P (2007) Nuclear size control in fission yeast. J Cell Biol 179:593–600
Nielsen R (2005) Molecular signatures of natural selection. Annu Rev Genet 39:197–218
Niu DK, Jiang L (2013) Can ENCODE tell us how much junk DNA we carry in our genome? Biochem Biophys Res Commun 430:1340–1343
Noleto RB, de Souza Fonseca Guimarães F, Paludo KS, Vicari MR, Artoni RF, Cestari MM (2009) Genome size evaluation in Tetraodontiform fishes from the Neotropical region. Mar Biotechnol 11:680–685
Ohno S (1972) So much “junk” DNA in our genome. Brookhaven Symp Biol 23:366–370
Ohno S (1973) Evolutional reason for having so much junk DNA. In: Pfeiffer RA (ed) Modern aspects of cytogenetics: constitutive heterochromatin in man. F. K. Schattauer Verlag, Stuttgart, pp 169–180
Ohshima K, Hattori M, Yada T, Gojobori T, Sakaki Y, Okada N (2003) Whole-genome screening indicates a possible burst of formation of processed pseudogenes and Alu repeats by particular L1 subfamilies in ancestral primates. Genome Biol 4:R74
Ohta T (1973) Slightly deleterious mutant substitutions in evolution. Nature 246:96–98
Oler AJ, Traina-Dorge S, Derbes RS, Canella D, Cairns BR, Roy-Engel AM (2012) Alu expression in human cell lines and their retrotranspositional potential. Mob DNA 3:11
Orgel LE, Crick FHC (1980) Selfish DNA: the ultimate parasite. Nature 284:604–607
Pagel M, Johnstone RA (1992) Variation across species in the size of the nuclear genome supports the junk-DNA explanation for the C-value paradox. Proc Roy Soc 249B:119–124
Palazzo AF, Gregory TR (2014) The case for junk DNA. PLoS Genet 10:e1004351
Parenteau J et al (2008) Deletion of many yeast introns reveals a minority of genes that require splicing for function. Mol Biol Cell 19:1932–1941
Pasyukova EG, Nuzhdin SV, Morozova TV, Mackay TF (2004) Accumulation of transposable elements in the genome of Drosophila melanogaster is associated with a decrease in fitness. J Hered 95:284–290
Pei B et al (2012) The GENCODE pseudogene resource. Genome Biol 13:R51
Peierls R (1960) Wolfgang Ernst Pauli, 1900-1958. Biogr Mem Fellows R Soc 5:174–192
Pellicier J, Fay MF, Leitch IJ (2010) The largest eukaryotic genome of them all? Bot J Linn Soc 164:10–15
Pertea M, Salzberg SL (2010) Between a chicken and a grape: estimating the number of human genes. Genome Biol 11:206
Petsko GA (2003) Funky, not junky. Genome Biol 4:104
Picot S, Wallau GL, Loreto EL, Heredia FO, Hua-Van A, Capy P (2008) The mariner transposable element in natural populations of Drosophila simulans. Heredity 101:53–59
Piegu B et al (2006) Doubling genome size without polyploidization: dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice. Genome Res 16:1262–1269
Ponjavic J, Ponting CP, Lunter G (2007) Functionality or transcriptional noise? Evidence for selection within long noncoding RNAs. Genome Res 17:556–565
Ponting CP, Hardison RC (2011) What fraction of the human genome is functional? Genome Res 21:1769–1776
Pruitt KD, Tatusova T, Klimke W, Maglott DR (2009) NCBI reference sequences: current status, policy and new initiatives. Nucleic Acids Res 37:D32–D36
Purves WK, Sadava D, Orians GH, Heller HC (2004) Life: the science of biology, 7th edn. Sinauer, Sunderland
Raj A, van Oudenaarden A (2008) Stochastic gene expression and its consequences. Cell 135:216–226
Rands CM, Meader S, Ponting CP, Lunter G (2014) PLoS Genet 10:e1004525
Rees H, Jones RN (1972) The origin of the wide species variation in nuclear DNA content. Int Rev Cytol 32:53–92
Rhind N et al (2011) Comparative functional genomics of the fission yeasts. Science 332:930–936
Roach JC et al (2010) Analysis of genetic inheritance in a family quartet by whole-genome sequencing. Science 328:636–639
Roest Crollius H et al (2000) Characterization and repeat analysis of the compact genome of the freshwater pufferfish Tetraodon nigroviridis. Genome Res 10:939–949
Schaack S, Gilbert C, Feschotte C (2010) Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution. Trends Ecol Evol 25:537–546
Šmarda P, Hejcman M, Březinová A, Horová L, Steigerová H, Zedek F, Bureš P, Hejcmanová P, Schellberg J (2013) Effect of phosphorus availability on the selection of species with different ploidy levels and genome sizes in a long-term grassland fertilization experiment. New Phytol 200:911–921
Smith NG, Brandström M, Ellegren H (2004) Evidence for turnover of functional noncoding DNA in mammalian genome evolution. Genomics 84:806–813
Srivastava M et al (2008) The Trichoplax genome and the nature of placozoans. Nature 454:955–960
Stamatoyannopoulos JA (2012) What does our genome encode? Genome Res 22:1602–1611
Starostova Z, Kratochvil L, Flajshans M (2008) Cell size does not always correspond to genome size: phylogenetic analysis in geckos questions optimal DNA theories of genome size evolution. Zoology 111:377–384
Starostova Z, Kubicka L, Konarzewski M, Kozlowski J, Kratochvil L (2009) Cell size but not genome size affects scaling of metabolic rate in eyelid geckos. Am Nat 174:E100–E105
Stevenson RL (1886) Strange case of Dr. Jekyll and Mr. Hyde. Charles Scribner’s Sons, New York. https://books.google.com/books?id=xZHv4CWgWaEC&printsec=frontcover&dq=jekyll+hyde&hl=en&sa=X&ei=uW6LVL2KKsGpgwSM4oHgCQ&ved=0CB4Q6wEwAA#v=onepage&q=jekyll%20hyde&f=false
Struhl K (2007) Transcriptional noise and the fidelity of initiation by RNA polymerase II. Nat Struct Mol Biol 14:103–105
Sulem P et al (2015) Identification of a large set of rare complete human knockouts. Nat Genet. https://doi.org/10.1038/ng.3243
Sundaram V et al (2014) Widespread contribution of transposable elements to the innovation of gene regulatory networks. Genome Res 24:1963–1976
Sunyaev S, Ramensky V, Koch I, Lathe W, Kondrashov AS, Bork P (2001) Prediction of deleterious human alleles. Hum Mol Genet 10:591–597
Swift H (1950) The constancy of deoxyribose nucleic acid in plant nuclei. Proc Natl Acad Sci U S A 36:643–654
Tang D (2015) Repetitive elements in vertebrate genomes. http://davetang.org/muse/2014/05/22/repetitive-elements-in-vertebrate-genomes/
Tenaillon MI, Hollister JD, Gaut BS (2010) A triptych of the evolution of plant transposable elements. Trends Plant Sci 15:471–478
Tennessen JA et al (2012) Evolution and functional impact of rare coding variation from deep sequencing of human exomes. Science 337:64–69
Thomas CA (1971) The genetic organization of chromosomes. Annu Rev Genet 5:237–256
Tishkoff SA et al (2006) Convergent adaptation of human lactase persistence in Africa and Europe. Nat Genet 39:31–40
Umylny B, Presting G, Ward WS (2007) Evidence of Alu and B1 expression in dbEST. Syst Biol Reprod Med 53:207–218
Van Valen LM, Maiorana VC (1991) Hela, a new microbial species. Evol Theor 10:71–74
Vitti JJ, Grossman SR, Sabeti PC (2013) Detecting natural selection in genomic data. Annu Rev Genet 47:97–120
Vogel F (1964) A preliminary estimate of the number of human genes. Nature 201:847
Ward LD, Kellis M (2012) Evidence of abundant purifying selection in humans for recently acquired regulatory functions. Science 337:1675–1678
Wardrop SL, kConFab Investigators, Brown MA (2005) Identification of two evolutionarily conserved and functional regulatory elements in intron 2 of the human BRCA1 gene. Genomics 86:316–328
Wen Y-Z, Zheng L-L, Qu L-H, Ayala FJ, Lun Z-R (2012) Pseudogenes are not pseudo any more. RNA Biol 9:27–32
Williamson SH, Hubisz MJ, Clark AG, Payseur BA, Bustamante CD, Nielsen R (2007) Localizing recent adaptive evolution in the human genome. PLoS Genet 3:e90
Wilson BA, Masel J (2011) Putatively noncoding transcripts show extensive association with ribosomes. Genome Biol Evol 3:1245–1252
Xue Y et al (2009) Human Y chromosome base-substitution mutation rate measured by direct sequencing in a deep-rooting pedigree. Curr Biol 19:1453–1457
Zeng K, Fu Y-X, Shi S, Wu C-I (2006) Statistical tests for detecting positive selection by utilizing high-frequency variants. Genetics 174:1431–1439
Zhou H, Zhao J, Yu CH, Luo QJ, Chen YQ, Xiao Y, Qu LH (2004) Identification of a novel box C/D snoRNA from mouse nucleolar cDNA library. Gene 327:99–105
Zimmer C (2015) Is most of our DNA garbage? New York Times http://www.nytimes.com/2015/03/08/magazine/is-most-of-our-dna-garbage.html?_r=0
Zuckerkandl E (1976) Gene control in eukaryotes and the C-value paradox: “excess” DNA as an impediment to transcription of coding sequences. J Mol Evol 9:73–104
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Graur, D. (2017). Rubbish DNA: The Functionless Fraction of the Human Genome. In: Saitou, N. (eds) Evolution of the Human Genome I. Evolutionary Studies. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56603-8_2
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