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Exaptation at the molecular genetic level

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Abstract

The realization that body parts of animals and plants can be recruited or coopted for novel functions dates back to, or even predates the observations of Darwin. S.J. Gould and E.S. Vrba recognized a mode of evolution of characters that differs from adaptation. The umbrella term aptation was supplemented with the concept of exaptation. Unlike adaptations, which are restricted to features built by selection for their current role, exaptations are features that currently enhance fitness, even though their present role was not a result of natural selection. Exaptations can also arise from nonaptations; these are characters which had previously been evolving neutrally. All nonaptations are potential exaptations. The concept of exaptation was expanded to the molecular genetic level which aided greatly in understanding the enormous potential of neutrally evolving repetitive DNA—including transposed elements, formerly considered junk DNA—for the evolution of genes and genomes. The distinction between adaptations and exaptations is outlined in this review and examples are given. Also elaborated on is the fact that such distinctions are sometimes more difficult to determine; this is a widespread phenomenon in biology, where continua abound and clear borders between states and definitions are rare.

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References

  • Ahituv, N., Zhu, Y., Visel, A., Holt, A., Afzal, V., Pennacchio, L.A., and Rubin, E.M. (2007). Deletion of ultraconserved elements yields viable mice. PLoS Biol 5, e234.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson, S.N., and Springer, N.M. (2018). Potential roles for transposable elements in creating imprinted expression. Curr Opin Genets Dev 49, 8–14.

    Article  CAS  Google Scholar 

  • Atkins, J.F., Gesteland, R.F., and Cech, T.R. (2011). RNA Worlds: from life’s origins to diversity in gene regulation (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).

    Google Scholar 

  • Babatz, T.D., and Burns, K.H. (2013). Functional impact of the human mobilome. Curr Opin Genets Dev 23, 264–270.

    Article  CAS  Google Scholar 

  • Baertsch, R., Diekhans, M., Kent, W.J., Haussler, D., and Brosius, J. (2008). Retrocopy contributions to the evolution of the human genome. BMC Genomics 9, 466.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bakel, H.V., Nislow, C., Blencowe,B.,J., and Hughes, T.R. (2011). Response to “The Reality of Pervasive Transcription”. PLoS Biol 9, e1001102.

    Article  CAS  PubMed Central  Google Scholar 

  • Barcroft, J., and Stephens, J.G. (1927). Observations upon the size of the spleen. J Physiol 64, 1–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Betrán, E., Thornton, K., and Long, M. (2002). Retroposed new genes out of the X in Drosophila. Genome Res 12, 1854–1859.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Black, S.G., Arnaud, F., Palmarini, M., and Spencer, T.E. (2010). Endogenous retroviruses in trophoblast differentiation and placental development. Am J Reprod Immunol 64, 255–264.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bladon, T.S., and McBurney, M.W. (1991). The rodent B2 sequence can affect expression when present in the transcribed region of a reporter gene. Gene 98, 259–263.

    Article  CAS  PubMed  Google Scholar 

  • Blain, J.C., and Szostak, J.W. (2014). Progress toward synthetic cells. Annu Rev Biochem 83, 615–640.

    Article  CAS  PubMed  Google Scholar 

  • Blond, J.L., Lavillette, D., Cheynet, V., Bouton, O., Oriol, G., Chapel-Fernandes, S., Mandrand, B., Mallet, F., and Cosset, F.L. (2000). An envelope glycoprotein of the human endogenous retrovirus HERV-W is expressed in the human placenta and fuses cells expressing the type D mammalian retrovirus receptor. J Virol 74, 3321–3329.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bobay, L.M., Touchon, M., and Rocha, E.P.C. (2014). Pervasive domestication of defective prophages by bacteria. Proc Natl Acad Sci USA 111, 12127–12132.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bock, R. (2017). Witnessing genome evolution: experimental reconstruction of endosymbiotic and horizontal gene transfer. Annu Rev Genet 51, 1–22.

    Article  CAS  PubMed  Google Scholar 

  • Boer, P.H., Adra, C.N., Lau, Y.F., and McBurney, M.W. (1987). The testisspecific phosphoglycerate kinase gene pgk-2 is a recruited retroposon.. Mol Cell Biol 7, 3107–3112.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bornberg-Bauer, E., and Albà, M.M. (2013). Dynamics and adaptive benefits of modular protein evolution. Curr Opin Struct Biol 23, 459–466.

    Article  CAS  PubMed  Google Scholar 

  • Bornberg-Bauer, E., Huylmans, A.K., and Sikosek, T. (2010). How do new proteins arise? Curr Opin Struct Biol 20, 390–396.

    Article  CAS  PubMed  Google Scholar 

  • Bornberg-Bauer, E., Schmitz, J., and Heberlein, M. (2015). Emergence of de novo proteins from ‘dark genomic matter’ by ‘grow slow and moult’. Biochem Soc Trans 43, 867–873.

    Article  CAS  PubMed  Google Scholar 

  • Bouttier, M., Laperriere, D., Memari, B., Mangiapane, J., Fiore, A., Mitchell, E., Verway, M., Behr, M.A., Sladek, R., Barreiro, L.B., et al. (2016). Alu repeats as transcriptional regulatory platforms in macrophage responses to M. tuberculosis infection. Nucleic Acids Res 44, 10571–10587.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bridges, C.B. (1936). The bar “gene” a duplication. Science 83, 210–211.

    Article  CAS  PubMed  Google Scholar 

  • Britten, R.J., and Davidson, E.H. (1969). Gene regulation for higher cells: a theory. Science 165, 349–357.

    Article  CAS  PubMed  Google Scholar 

  • Brosius, J. (1991). Retroposons—seeds of evolution. Science 251, 753.

    Article  CAS  PubMed  Google Scholar 

  • Brosius, J. (1999a). Genomes were forged by massive bombardments with retroelements and retrosequences. Genetica 107, 209–238.

    Article  CAS  PubMed  Google Scholar 

  • Brosius, J. (1999b). Many G-protein-coupled receptors are encoded by retrogenes. Trends Genets 15, 304–305.

    Article  CAS  Google Scholar 

  • Brosius, J. (1999c). RNAs from all categories generate retrosequences that may be exapted as novel genes or regulatory elements. Gene 238, 115–134.

    Article  CAS  PubMed  Google Scholar 

  • Brosius, J. (2003a). The contribution of RNAs and retroposition to evolutionary novelties. Genetica 118, 99–115.

    Article  CAS  PubMed  Google Scholar 

  • Brosius, J. (2003b). Gene duplication and other evolutionary strategies: from the RNA world to the future. J Struct Funct Genomics 3, 1–17.

    Article  CAS  PubMed  Google Scholar 

  • Brosius, J. (2005a). Disparity, adaptation, exaptation, bookkeeping, and contingency at the genome level. Paleobiology 31, 1–16.

    Article  Google Scholar 

  • Brosius, J. (2005b). Echoes from the past—are we still in an RNP world? Cytogenet Genome Res 110, 8–24.

    Article  CAS  PubMed  Google Scholar 

  • Brosius, J. (2005c). Waste not, want not—transcript excess in multicellular eukaryotes. Trends Genets 21, 287–288.

    Article  CAS  Google Scholar 

  • Brosius, J. (2009). The fragmented gene. Ann New York Acad Sci 1178, 186–193.

    Article  CAS  Google Scholar 

  • Brosius, J. (2014). The persistent contributions of RNA to eukaryotic gen(om)e architecture and cellular function. Cold Spring Harbor Perspectives Biol 6, a016089.

    Book  Google Scholar 

  • Brosius, J., and Gould, S.J. (1992). On “genomenclature”: a comprehensive (and respectful) taxonomy for pseudogenes and other “junk DNA”. Proc Natl Acad Sci USA 89, 10706–10710.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brosius, J., and Raabe, C.A. (2016). What is an RNA? A top layer for RNA classification. RNA Biol 13, 140–144.

    Article  PubMed  PubMed Central  Google Scholar 

  • Brosius, J., and Tiedge, H. (1995). Reverse transcriptase: mediator of genomic plasticity. Virus Genes 11, 163–179.

    Article  CAS  PubMed  Google Scholar 

  • Buss, D.M., Haselton, M.G., Shackelford, T.K., Bleske, A.L., and Wakefield, J.C. (1998). Adaptations, exaptations, and spandrels. Am Psychol 53, 533–548.

    Article  CAS  PubMed  Google Scholar 

  • Cai, J., Zhao, R., Jiang, H., and Wang, W. (2008). De novo origination of a new protein-coding gene in Saccharomyces cerevisiae. Genetics 179, 487–496.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Capshew, C.R., Dusenbury, K.L., and Hundley, H.A. (2012). Inverted Alu dsRNA structures do not affect localization but can alter translation efficiency of human mRNAs independent of RNA editing. Nucleic Acids Res 40, 8637–8645.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carninci, P. (2010). RNA dust: where are the genes? DNA Res 17, 51–59.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carrieri, C., Cimatti, L., Biagioli, M., Beugnet, A., Zucchelli, S., Fedele, S., Pesce, E., Ferrer, I., Collavin, L., Santoro, C., et al. (2012). Long noncoding antisense RNA controls Uchl1 translation through an embedded SINEB2 repeat. Nature 491, 454–457.

    Article  CAS  PubMed  Google Scholar 

  • Carvunis, A.R., Rolland, T., Wapinski, I., Calderwood, M.A., Yildirim, M. A., Simonis, N., Charloteaux, B., Hidalgo, C.A., Barbette, J., Santhanam, B., et al. (2012). Proto-genes and de novo gene birth. Nature 487, 370–374.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caudron-Herger, M., Pankert, T., Seiler, J., Németh, A., Voit, R., Grummt, I., and Rippe, K. (2015). Alu element-containing RNAs maintain nucleolar structure and function. EMBO J 34, 2758–2774.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, H., Chen, L., Wu, Y., Shen, H., Yang, G., and Deng, C. (2017). The exonization and functionalization of an Alu-J element in the protein coding region of glycoprotein hormone alpha gene represent a novel mechanism to the evolution of hemochorial placentation in primates. Mol Biol Evol 34, 3216–3231.

    Article  CAS  PubMed  Google Scholar 

  • Chen, L.L., and Yang, L. (2017). ALU ternative regulation for gene expression. Trends Cell Biol 27, 480–490.

    Article  CAS  PubMed  Google Scholar 

  • Chen, S., Spletter, M., Ni, X., White, K.P., Luo, L., and Long, M. (2012). Frequent recent origination of brain genes shaped the evolution of foraging behavior in Drosophila. Cell Rep 1, 118–132.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, S., Zhang, Y.E., and Long, M. (2010). New genes in Drosophila quickly become essential. Science 330, 1682–1685.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, S., Krinsky, B.H., and Long, M. (2013). New genes as drivers of phenotypic evolution. Nat Rev Genet 14, 645–660.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, W., Heierhorst, J., Brosius, J., and Tiedge, H. (1997). Expression of neural BC1 RNA: induction in murine tumours. Eur J Cancer 33, 288–292.

    Article  CAS  PubMed  Google Scholar 

  • Chillon, I., and Pyle, A.M. (2016). Inverted repeat Alu elements in the human lincRNA-p21 adopt a conserved secondary structure that regulates RNA function. Nucleic Acids Res 44, 9462–9471.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chuong, E.B. (2013). Retroviruses facilitate the rapid evolution of the mammalian placenta. Bioessays 35, 853–861.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chuong, E.B., Elde, N.C., and Feschotte, C. (2016). Regulatory evolution of innate immunity through co-option of endogenous retroviruses. Science 351, 1083–1087.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chuong, E.B., Elde, N.C., and Feschotte, C. (2017). Regulatory activities of transposable elements: from conflicts to benefits. Nat Rev Genet 18, 71–86.

    Article  CAS  PubMed  Google Scholar 

  • Chuong, E.B., Rumi, M.A.K., Soares, M.J., and Baker, J.C. (2013). Endogenous retroviruses function as species-specific enhancer elements in the placenta. Nat Genet 45, 325–329.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Churakov, G., Sadasivuni, M.K., Rosenbloom, K.R., Huchon, D., Brosius, J., and Schmitz, J. (2010). Rodent evolution: back to the root. Mol Biol Evol 27, 1315–1326.

    Article  CAS  PubMed  Google Scholar 

  • (a)Clark, M.B., Amaral, P.P., Schlesinger, F.J., Dinger, M.E., Taft, R.J., Rinn, J.L., Ponting, C.P., Stadler, P.F., Morris, K.V., Morillon, A., et al. (2011). The reality of pervasive transcription. PLoS Biol 9, e1000625.; (b)discussion e1001102.

    Article  CAS  Google Scholar 

  • Daniel, C., Behm, M., and Öhman, M. (2015). The role of Alu elements in the cis-regulation of RNA processing. Cell Mol Life Sci 72, 4063–4076.

    Article  CAS  PubMed  Google Scholar 

  • Daniel, C., Silberberg, G., Behm, M., and Öhman, M. (2014). Alu elements shape the primate transcriptome by cis-regulation of RNA editing. Genome Biol 15, R28.

    Google Scholar 

  • Darwin, C. (1845). Journal of researches into the natural history and geology of the countries visited during the voyage of H.M.S. Beagle round the world, under the Command of Capt. Fitz Roy, R.N Second edn (London: John Murray).

    Google Scholar 

  • Darwin, C. (1972). On the Origin of Species, 6th edn (London: John Murray).

    Google Scholar 

  • de Koning, A.P.J., Gu, W., Castoe, T.A., Batzer, M.A., and Pollock, D.D. (2011). Repetitive elements may comprise over two-thirds of the human genome. PLoS Genet 7, e1002384.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Souza, F.S., Franchini, L.F., and Rubinstein, M. (2013). Exaptation of transposable elements into novel cis-regulatory elements: is the evidence always strong? Mol Biol Evol 30, 1239–1251.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dechiara, T.M., and Brosius, J. (1987). Neural BC1 RNA: cDNA clones reveal nonrepetitive sequence content.. Proc Natl Acad Sci USA 84, 2624–2628.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deininger, P.L., Tiedge, H., Kim, J., and Brosius, J. (1996). Evolution, expression, and possible function of a master gene for amplification of an interspersed repeated DNA family in rodents. Prog Nucleic Acid Re 52, 67–88.

    Article  CAS  Google Scholar 

  • del Rosario, R.C.H., Rayan, N.A., and Prabhakar, S. (2014). Noncoding origins of anthropoid traits and a new null model of transposon functionalization. Genome Res 24, 1469–1484.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dennett, D.C. (1995). Darwin’s Dangerous Idea (New York: Simon & Schuster).

    Google Scholar 

  • Dewannieux, M., and Heidmann, T. (2005). LINEs, SINEs and processed pseudogenes: parasitic strategies for genome modeling. Cytogenet Genome Res 110, 35–48.

    Article  CAS  PubMed  Google Scholar 

  • Dewannieux, M., and Heidmann, T. (2013). Endogenous retroviruses: acquisition, amplification and taming of genome invaders. Curr Opin Virol 3, 646–656.

    Article  CAS  PubMed  Google Scholar 

  • Dickel, D.E., Ypsilanti, A.R., Pla, R., Zhu, Y., Barozzi, I., Mannion, B.J., Khin, Y.S., Fukuda-Yuzawa, Y., Plajzer-Frick, I., Pickle, C.S., et al. (2018). Ultraconserved enhancers are required for normal development. Cell 172, 491–499.e15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding, Y., Zhao, L., Yang, S., Jiang, Y., Chen, Y., Zhao, R., Zhang, Y., Zhang, G., Dong, Y., Yu, H., et al. (2010). A young Drosophila duplicate gene plays essential roles in spermatogenesis by regulating several Y-linked male fertility genes. PLoS Genet 6, e1001255.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doolittle, W.F., and Sapienza, C. (1980). Selfish genes, the phenotype paradigm and genome evolution. Nature 284, 601–603.

    Article  CAS  PubMed  Google Scholar 

  • Drezen, J.M., Gauthier, J., Josse, T., Bézier, A., Herniou, E., and Huguet, E. (2017). Foreign DNA acquisition by invertebrate genomes. J Invertebrate Pathol 147, 157–168.

    Article  CAS  Google Scholar 

  • Dupressoir, A., Lavialle, C., and Heidmann, T. (2012). From ancestral infectious retroviruses to bona fide cellular genes: role of the captured syncytins in placentation. Placenta 33, 663–671.

    Article  CAS  PubMed  Google Scholar 

  • Eisenberg, E. (2016). Proteome diversification by genomic parasites. Genome Biol 17, 17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elbarbary, R.A., Lucas, B.A., and Maquat, L.E. (2016). Retrotransposons as regulators of gene expression. Science 351, aac7247.

    Google Scholar 

  • Elbarbary, R.A., and Maquat, L.E. (2017). Distinct mechanisms obviate the potentially toxic effects of inverted-repeat Alu elements on cellular RNA metabolism. Nat Struct Mol Biol 24, 496–498.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ellison, C.E., and Bachtrog, D. (2013). Dosage compensation via transposable element mediated rewiring of a regulatory network. Science 342, 846–850.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Emera, D., Casola, C., Lynch, V.J., Wildman, D.E., Agnew, D., and Wagner, G.P. (2012). Convergent evolution of endometrial prolactin expression in primates, mice, and elephants through the independent recruitment of transposable elements. Mol Biol Evol 29, 239–247.

    Article  CAS  PubMed  Google Scholar 

  • Emera, D., Yin, J., Reilly, S.K., Gockley, J., and Noonan, J.P. (2016). Origin and evolution of developmental enhancers in the mammalian neocortex. Proc Natl Acad Sci USA 113, e2617–E2626.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Estécio, M.R.H., Gallegos, J., Dekmezian, M., Lu, Y., Liang, S., and Issa, J. P.J. (2012). SINE retrotransposons cause epigenetic reprogramming of adjacent gene promoters. Mol Cancer Res 10, 1332–1342.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farré, D., Engel, P., and Angulo, A. (2016). Novel role of 3′UTR-embedded Alu elements as facilitators of processed pseudogene genesis and host gene capture by viral genomes. PLoS ONE 11, e0169196.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Faulkner, G.J., Kimura, Y., Daub, C.O., Wani, S., Plessy, C., Irvine, K.M., Schroder, K., Cloonan, N., Steptoe, A.L., Lassmann, T., et al. (2009). The regulated retrotransposon transcriptome of mammalian cells. Nat Genet 41, 563–571.

    Article  CAS  PubMed  Google Scholar 

  • Fielder, D.P. (2012). Seasonal and diel dive performance and behavioral ecology of the bimodally respiring freshwater turtle Myuchelys bellii of eastern Australia. J Comp Physiol A 198, 129–143.

    Article  Google Scholar 

  • Fuentes, D.R., Swigut, T., and Wysocka, J. (2018). Systematic perturbation of retroviral LTRs reveals widespread long-range effects on human gene regulation. Elife 7, pii: e35989.

    Book  Google Scholar 

  • Galindo-González, L., Mhiri, C., Deyholos, M.K., and Grandbastien, M.A. (2017). LTR-retrotransposons in plants: Engines of evolution. Gene 626, 14–25.

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Perez, J.L., Widmann, T.J., and Adams, I.R. (2016). The impact of transposable elements on mammalian development. Development 143, 4101–4114.

    Article  CAS  PubMed  Google Scholar 

  • Gardiner, D.M., Kazan, K., and Manners, J.M. (2013). Cross-kingdom gene transfer facilitates the evolution of virulence in fungal pathogens. Plant Sci 210, 151–158.

    Article  CAS  PubMed  Google Scholar 

  • Gavelis, G.S., Keeling, P.J., and Leander, B.S. (2017). How exaptations facilitated photosensory evolution: Seeing the light by accident. Bioessays 39.

    Google Scholar 

  • Ge, S.X. (2017). Exploratory bioinformatics investigation reveals importance of “junk” DNA in early embryo development. BMC Genomics 18, 200.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghaly, T.M., and Gillings, M.R. (2018). Mobile DNAs as ecologically and evolutionarily independent units of life. Trends Microbiol 26, 904–912.

    Article  CAS  PubMed  Google Scholar 

  • Gilbert-Kawai, E.T., Milledge, J.S., Grocott, M.P., and Martin, D.S. (2014). King of the mountains: Tibetan and Sherpa physiological adaptations for life at high altitude. Physiology (Bethesda) 29, 388–402.

    CAS  Google Scholar 

  • Gladyshev, E.A., Meselson, M., and Arkhipova, I.R. (2008). Massive horizontal gene transfer in bdelloid rotifers. Science 320, 1210–1213.

    Article  CAS  PubMed  Google Scholar 

  • Glinsky, G.V. (2015). Transposable elements and DNA methylation create in embryonic stem cells human-specific regulatory sequences associated with distal enhancers and noncoding RNAs. Genome Biol Evol 7, 1432–1454.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gophna, U., Charlebois, R.L., and Doolittle, W.F. (2006). Ancient lateral gene transfer in the evolution of Bdellovibrio bacteriovorus. Trends MicroBiol 14, 64–69.

    Article  CAS  PubMed  Google Scholar 

  • Gould, S.J. (1991). Exaptation: a crucial tool for an evolutionary psychology. J Social Issues 47, 43–65.

    Article  Google Scholar 

  • Gould, S.J. (2002). The Structure of Evolutionary Theory (Cambridge, MA: Belknap, Harvard University Press).

    Book  Google Scholar 

  • Gould, S.J., and Lewontin, R.C. (1979). The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc R Soc B-Biol Sci 205, 581–598.

    Article  CAS  Google Scholar 

  • Gould, S.J., and Vrba, E.S. (1982). Exaptation—a missing term in the science of form. Paleobiology 8, 4–15.

    Article  Google Scholar 

  • Gubala, A.M., Schmitz, J.F., Kearns, M.J., Vinh, T.T., Bornberg-Bauer, E., Wolfner, M.F., and Findlay, G.D. (2017). The Goddard and Saturn genes are essential for Drosophila male fertility and may have arisen de novo. Mol Biol Evol 34, 1066–1082.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Haig, D. (2016). Transposable elements: Self-seekers of the germline, team-players of the soma. BioEssays 38, 1158–1166.

    Article  CAS  PubMed  Google Scholar 

  • Hall, J.P.J., Brockhurst, M.A., and Harrison, E. (2017). Sampling the mobile gene pool: innovation via horizontal gene transfer in bacteria. Philos Trans R Soc Lond B Biol Sci 372, pii: 20160424.

    Google Scholar 

  • Harmston, N., Baresic, A., and Lenhard, B. (2013). The mystery of extreme non-coding conservation. Philos Trans R Soc B-Biol Sci 368, 20130021.

    Article  CAS  Google Scholar 

  • Heinen, T.J.A.J., Staubach, F., Häming, D., and Tautz, D. (2009). Emergence of a new gene from an intergenic region. Curr Biol 19, 1527–1531.

    Article  CAS  PubMed  Google Scholar 

  • Hezroni, H., Ben-Tov Perry, R., Meir, Z., Housman, G., Lubelsky, Y., and Ulitsky, I. (2017). A subset of conserved mammalian long non-coding RNAs are fossils of ancestral protein-coding genes. Genome Biol 18, 162.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirsch, C.D., and Springer, N.M. (2017). Transposable element influences on gene expression in plants. Biochim Biophys Acta Gene Regul Mech 1860, 157–165.

    Article  CAS  PubMed  Google Scholar 

  • Hoffman, Y., Dahary, D., Bublik, D.R., Oren, M., and Pilpel, Y. (2013). The majority of endogenous microRNA targets within Alu elements avoid the microRNA machinery. Bioinformatics 29, 894–902.

    Article  CAS  PubMed  Google Scholar 

  • Hoffman, Y., Pilpel, Y., and Oren, M. (2014). microRNAs and Alu elements in the p53-Mdm2-Mdm4 regulatory network. J Mol Cell Biol 6, 192–197.

    CAS  PubMed  Google Scholar 

  • Holdt, L.M., Hoffmann, S., Sass, K., Langenberger, D., Scholz, M., Krohn, K., Finstermeier, K., Stahringer, A., Wilfert, W., Beutner, F., et al. (2013). Alu elements in ANRIL non-coding RNA at chromosome 9p21 modulate atherogenic cell functions through trans-regulation of gene networks. PLoS Genet 9, e1003588.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu, Q.D., Tanasa, B., Trabucchi, M., Li, W., Zhang, J., Ohgi, K.A., Rose, D.W., Glass, C.K., and Rosenfeld, M.G. (2012). DICER-and AGO3-dependent generation of retinoic acid-induced DR2 Alu RNAs regulates human stem cell proliferation. Nat Struct Mol Biol 19, 1168–1175.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huda, A., Mariño-Ramírez, L., and Jordan, I.K. (2010). Epigenetic histone modifications of human transposable elements: genome defense versus exaptation. Mobile DNA 1, 2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huda, A., Tyagi, E., Mariño-Ramírez, L., Bowen, N.J., Jjingo, D., and Jordan, I.K. (2011). Prediction of transposable element derived enhancers using chromatin modification profiles. PLoS ONE 6, e27513.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hunt, G.R., Gray, R.D., and Taylor, A.H. (2013). Why is tool use rare in animals? In Tool Use in Animals: Cognition and Ecology, C. Sanz, C. Boesch, and J. Call, eds. (Cambridge: Cambridge University Press), pp. 89–118.

    Google Scholar 

  • Husnik, F., and McCutcheon, J.P. (2018). Functional horizontal gene transfer from bacteria to eukaryotes. Nat Rev Micro 16, 67–79.

    Article  CAS  Google Scholar 

  • Ilardo, M.A., Moltke, I., Korneliussen, T.S., Cheng, J., Stern, A.J., Racimo, F., de Barros Damgaard, P., Sikora, M., Seguin-Orlando, A., Rasmussen, S., et al. (2018). Physiological and genetic adaptations to diving in sea nomads. Cell 173, 569–580.e15.

    Article  CAS  PubMed  Google Scholar 

  • Ivanova, E., Berger, A., Scherrer, A., Alkalaeva, E., and Strub, K. (2015). Alu RNA regulates the cellular pool of active ribosomes by targeted delivery of SRP9/14 to 40S subunits. Nucleic Acids Res 43, 2874–2887.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jacques, P.É., Jeyakani, J., and Bourque, G. (2013). The majority of primate-specific regulatory sequences are derived from transposable elements. PLoS Genet 9, e1003504.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeck, W.R., Sorrentino, J.A., Wang, K., Slevin, M.K., Burd, C.E., Liu, J., Marzluff, W.F., and Sharpless, N.E. (2013). Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 19, 141–157.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeffares, D.C., Poole, A.M., and Penny, D. (1998). Relics from the RNA world. J Mol Evol 46, 18–36.

    Article  CAS  PubMed  Google Scholar 

  • Jiang, L., Li, T., Zhang, X., Zhang, B., Yu, C., Li, Y., Fan, S., Jiang, X., Khan, T., Hao, Q., et al. (2017). RPL10L is required for male meiotic division by compensating for RPL10 during meiotic sex chromosome inactivation in mice. Curr Biol 27, 1498–1505.e6.

    Article  CAS  PubMed  Google Scholar 

  • Joly-Lopez, Z., and Bureau, T.E. (2018). Exaptation of transposable element coding sequences. Curr Opin Genets Dev 49, 34–42.

    Article  CAS  Google Scholar 

  • Jørgensen, C.B. (1998). Role of urinary and cloacal bladders in chelonian water economy: historical and comparative perspectives. Biol Rev 73, 347–366.

    Article  PubMed  Google Scholar 

  • Joyce, G.F., and Szostak, J.W. (2018). Protocells and RNA self-replication. Cold Spring Harb Perspect Biol 10, pii: a034801.

    Book  Google Scholar 

  • Jung, J., Lee, S., Cho, H.S., Park, K., Ryu, J.W., Jung, M., Kim, J., Kim, H., and Kim, D.S. (2018). Bioinformatic analysis of regulation of natural antisense transcripts by transposable elements in human mRNA. Genomics, pii: S0888-7543(18)30025-9.

    Google Scholar 

  • Kapusta, A., Kronenberg, Z., Lynch, V.J., Zhuo, X., Ramsay, L.A., Bourque, G., Yandell, M., and Feschotte, C. (2013). Transposable elements are major contributors to the origin, diversification, and regulation of vertebrate long noncoding RNAs. PLoS Genet 9, e1003470.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelley, D., and Rinn, J. (2012). Transposable elements reveal a stem cellspecific class of long noncoding RNAs. Genome Biol 13, R107.

    Google Scholar 

  • Kelley, D.R., Hendrickson, D.G., Tenen, D., and Rinn, J.L. (2014). Transposable elements modulate human RNA abundance and splicing via specific RNA-protein interactions. Genome Biol 15, 537.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kemkemer, C., and Long, M. (2014). New genes important for development. EMBO Rep 15, 460–461.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kent, W.J., Baertsch, R., Hinrichs, A., Miller, W., and Haussler, D. (2003). Evolution’s cauldron: Duplication, deletion, and rearrangement in the mouse and human genomes. Proc Natl Acad Sci USA 100, 11484–11489.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keren, H., Lev-Maor, G., and Ast, G. (2010). Alternative splicing and evolution: diversification, exon definition and function. Nat Rev Genet 11, 345–355.

    Article  CAS  PubMed  Google Scholar 

  • Khanam, T., Rozhdestvensky, T.S., Bundman, M., Galiveti, C.R., Handel, S., Sukonina, V., Jordan, U., Brosius, J., and Skryabin, B.V. (2007). Two primate-specific small non-protein-coding RNAs in transgenic mice: neuronal expression, subcellular localization and binding partners. Nucleic Acids Res 35, 529–539.

    Article  CAS  PubMed  Google Scholar 

  • Kim, E., Goren, A., and Ast, G. (2008). Alternative splicing and disease. RNA Biol 5, 17–19.

    Article  CAS  PubMed  Google Scholar 

  • Kim, Y.J., Lee, J., and Han, K. (2012). Transposable elements: no more ‘junk DNA’. Genomics Inform 10, 226–233.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kingsolver, J.G., and Koehl, M.A.R. (1985). Aerodynamics, thermoregulation, and the evolution of insect wings: differential scaling and evolutionary change. Evolution 39, 488–504.

    Article  PubMed  Google Scholar 

  • Klasberg, S., Bitard-Feildel, T., Callebaut, I., and Bornberg-Bauer, E. (2018). Origins and structural properties of novel and de novo protein domains during insect evolution. FEBS J 285, 2605–2625.

    Article  CAS  PubMed  Google Scholar 

  • Koch, A.L. (1972). Enzyme evolution. I. The importance of untranslatable intermediates. Genetics 72, 297–316.

    CAS  PubMed  Google Scholar 

  • Kondrashov, A.V., Kiefmann, M., Ebnet, K., Khanam, T., Muddashetty, R. S., and Brosius, J. (2005). Inhibitory effect of naked neural BC1 RNA or BC200 RNA on eukaryotic in vitro translation systems is reversed by poly(A)-binding protein (PABP). J Mol Biol 353, 88–103.

    Article  CAS  PubMed  Google Scholar 

  • Koonin, E.V. (2016). Horizontal gene transfer: essentiality and evolvability in prokaryotes, and roles in evolutionary transitions. F1000Res 5, pii: F1000 Faculty Rev-1805.

    Google Scholar 

  • Koonin, E.V., and Krupovic, M. (2018). The depths of virus exaptation. Curr Opin Virol 31, 1–8.

    Article  CAS  PubMed  Google Scholar 

  • Kriegs, J.O., Schmitz, J., Makalowski, W., and Brosius, J. (2005). Does the AD7c-NTP locus encode a protein? Biochim Biophys Acta 1727, 1–4.

    Article  CAS  PubMed  Google Scholar 

  • Krull, M., Brosius, J., and Schmitz, J. (2005). Alu-SINE exonization: en route to protein-coding function. Mol Biol Evol 22, 1702–1711.

    Article  CAS  PubMed  Google Scholar 

  • Krull, M., Petrusma, M., Makalowski, W., Brosius, J., and Schmitz, J. (2007). Functional persistence of exonized mammalian-wide interspersed repeat elements (MIRs). Genome Res 17, 1139–1145.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuryshev, V.Y., Skryabin, B.V., Kremerskothen, J., Jurka, J., and Brosius, J. (2001). Birth of a gene: locus of neuronal BC200 snmRNA in three prosimians and human BC200 pseudogenes as archives of change in the Anthropoidea lineage. J Mol Biol 309, 1049–1066.

    Article  CAS  PubMed  Google Scholar 

  • Lacroix, B., and Citovsky, V. (2018). Beyond agrobacterium-mediated transformation: horizontal gene transfer from bacteria to eukaryotes. Curr Top Microbiol Immunol 418, 443–462.

    CAS  PubMed  Google Scholar 

  • Larsen, P.A., Hunnicutt, K.E., Larsen, R.J., Yoder, A.D., and Saunders, A. M. (2018). Warning SINEs: Alu elements, evolution of the human brain, and the spectrum of neurological disease. Chromosome Res 26, 93–111.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larson, G., Stephens, P.A., Tehrani, J.J., and Layton, R.H. (2013). Exapting exaptation. Trends Ecol Evol 28, 497–498.

    Article  PubMed  Google Scholar 

  • Lavi, E., and Carmel, L. (2018). Alu exaptation enriches the human transcriptome by introducing new gene ends. RNA Biol 15, 715–725.

    PubMed  PubMed Central  Google Scholar 

  • Lee, H.E., Ayarpadikannan, S., and Kim, H.S. (2015). Role of transposable elements in genomic rearrangement, evolution, gene regulation and epigenetics in primates. Genes Genet Syst 90, 245–257.

    Article  CAS  PubMed  Google Scholar 

  • Lev-Maor, G., Sorek, R., Shomron, N., and Ast, G. (2003). The birth of an alternatively spliced exon: 3′ splice-site selection in Alu exons. Science 300, 1288–1291.

    Article  CAS  PubMed  Google Scholar 

  • Levy, A., Sela, N., and Ast, G. (2008). TranspoGene and microTranspoGene: transposed elements influence on the transcriptome of seven vertebrates and invertebrates. Nucleic Acids Res 36, D47–D52.

    Google Scholar 

  • Lewejohann, L., Skryabin, B.V., Sachser, N., Prehn, C., Heiduschka, P., Thanos, S., Jordan, U., Dell’Omo, G., Vyssotski, A.L., Pleskacheva, M. G., et al. (2004). Role of a neuronal small non-messenger RNA: behavioural alterations in BC1 RNA-deleted mice. Behavioural Brain Res 154, 273–289.

    Article  CAS  Google Scholar 

  • Lewis, E.B. (1951). Pseudoallelism and gene evolution. Cold Spring Harb Symp Quant Biol 16, 159–174.

    Article  CAS  PubMed  Google Scholar 

  • Li, D., Dong, Y., Jiang, Y., Jiang, H., Cai, J., and Wang, W. (2010). A de novo originated gene depresses budding yeast mating pathway and is repressed by the protein encoded by its antisense strand. Cell Res 20, 408–420.

    Article  CAS  PubMed  Google Scholar 

  • Li, X., Liang, J., Yu, H., Su, B., Xiao, C., Shang, Y., and Wang, W. (2007). Functional consequences of new exon acquisition in mammalian chromodomain Y-like (CDYL) genes. Trends Genets 23, 427–431.

    Article  CAS  Google Scholar 

  • Liang, K.H., and Yeh, C.T. (2013). A gene expression restriction network mediated by sense and antisense Alu sequences located on proteincoding messenger RNAs. BMC Genomics 14, 325.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin, L., Jiang, P., Park, J.W., Wang, J., Lu, Z.X., Lam, M.P.Y., Ping, P., and Xing, Y. (2016). The contribution of Alu exons to the human proteome. Genome Biol 17, 15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Long, M., Betrán, E., Thornton, K., and Wang, W. (2003a). The origin of new genes: glimpses from the young and old. Nat Rev Genet 4, 865–875.

    Article  CAS  PubMed  Google Scholar 

  • Long, M. (2003b). Origin of new genes: evidence from experimental and computational analyses. Genetica 118, 171–182.

    Article  CAS  PubMed  Google Scholar 

  • Long, M., and Langley, C.H. (1993). Natural selection and the origin of jingwei, a chimeric processed functional gene in Drosophila. Science 260, 91–95.

    Article  CAS  PubMed  Google Scholar 

  • Long, M., VanKuren, N.W., Chen, S., and Vibranovski, M.D. (2013). New gene evolution: little did we know. Annu Rev Genet 47, 307–333.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lowe, C.B., and Haussler, D. (2012). 29 mammalian genomes reveal novel exaptations of mobile elements for likely regulatory functions in the human genome. PLoS ONE 7, e43128.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lubelsky, Y., and Ulitsky, I. (2018). Sequences enriched in Alu repeats drive nuclear localization of long RNAs in human cells. Nature 555, 107–111.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lucas, B.A., Lavi, E., Shiue, L., Cho, H., Katzman, S., Miyoshi, K., Siomi, M.C., Carmel, L., Ares Jr., M., and Maquat, L.E. (2018). Evidence for convergent evolution of SINE-directed Staufen-mediated mRNA decay. Proc Natl Acad Sci USA 115, 968–973.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ludwig, A., Rozhdestvensky, T.S., Kuryshev, V.Y., Schmitz, J., and Brosius, J. (2005). An unusual primate locus that attracted two independent Alu insertions and facilitates their transcription. J Mol Biol 350, 200–214.

    Article  CAS  PubMed  Google Scholar 

  • Lunyak, V.V., Prefontaine, G.G., Núñez, E., Cramer, T., Ju, B.G., Ohgi, K. A., Hutt, K., Roy, R., García-Díaz, A., Zhu, X., et al. (2007). Developmentally regulated activation of a SINE B2 repeat as a domain boundary in organogenesis. Science 317, 248–251.

    Article  CAS  PubMed  Google Scholar 

  • Lynch, V.J., Nnamani, M.C., Kapusta, A., Brayer, K., Plaza, S.L., Mazur, E. C., Emera, D., Sheikh, S.Z., Grützner, F., Bauersachs, S., et al. (2015). Ancient transposable elements transformed the uterine regulatory landscape and transcriptome during the evolution of mammalian pregnancy. Cell Rep 10, 551–561.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Makałowski, W., Mitchell, G.A., and Labuda, D. (1994). Alu sequences in the coding regions of mRNA: a source of protein variability. Trends Genets 10, 188–193.

    Article  Google Scholar 

  • Mandal, A.K., Pandey, R., Jha, V., and Mukerji, M. (2013). Transcriptome-wide expansion of non-coding regulatory switches: evidence from cooccurrence of Alu exonization, antisense and editing. Nucleic Acids Res 41, 2121–2137.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martignetti, J.A., and Brosius, J. (1993a). BC200 RNA: a neural RNA polymerase III product encoded by a monomeric Alu element.. Proc Natl Acad Sci USA 90, 11563–11567.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martignetti, J.A., and Brosius, J. (1993b). Neural BC1 RNA as an evolutionary marker: guinea pig remains a rodent. Proc Natl Acad Sci USA 90, 9698–9702.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martignetti, J.A., and Brosius, J. (1995). BC1 RNA: transcriptional analysis of a neural cell-specific RNA polymerase III transcript.. Mol Cell Biol 15, 1642–1650.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin, W.F. (2017). Too much eukaryote LGT. Bioessays 39.

    Book  Google Scholar 

  • Matsui, H., Hunt, G.R., Oberhofer, K., Ogihara, N., McGowan, K.J., Mithraratne, K., Yamasaki, T., Gray, R.D., and Izawa, E. (2016). Adaptive bill morphology for enhanced tool manipulation in New Caledonian crows. Sci Rep 6, 22776.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCarrey, J.R., and Thomas, K. (1987). Human testis-specific PGK gene lacks introns and possesses characteristics of a processed gene. Nature 326, 501–505.

    Article  CAS  PubMed  Google Scholar 

  • McLaughlin, R.N., Young, J.M., Yang, L., Neme, R., Wichman, H.A., and Malik, H.S. (2014). Positive selection and multiple losses of the LINE-1-derived L1TD1 gene in mammals suggest a dual role in genome defense and pluripotency. PLoS Genet 10, e1004531.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Medstrand, P., Landry, J.R., and Mager, D.L. (2001). Long terminal repeats are used as alternative promoters for the endothelin B receptor and apolipoprotein C-I genes in humans. J Biol Chem 276, 1896–1903.

    Article  CAS  PubMed  Google Scholar 

  • Méheust, R., Watson, A.K., Lapointe, F.J., Papke, R.T., Lopez, P., and Bapteste, E. (2018). Hundreds of novel composite genes and chimeric genes with bacterial origins contributed to haloarchaeal evolution. Genome Biol 19, 75.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mi, S., Lee, X., Li, X., Veldman, G.M., Finnerty, H., Racie, L., LaVallie, E., Tang, X.Y., Edouard, P., Howes, S., et al. (2000). Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403, 785–789.

    Article  CAS  PubMed  Google Scholar 

  • Mo, D., Raabe, C.A., Reinhardt, R., Brosius, J., and Rozhdestvensky, T.S. (2013). Alternative processing as evolutionary mechanism for the origin of novel nonprotein coding RNAs. Genome Biol Evol 5, 2061–2071.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monte, S.M., Ghanbari, K., Frey, W.H., Beheshti, I., Averback, P., Hauser, S.L., Ghanbari, H.A., and Wands, J.R. (1997). Characterization of the AD7C-NTP cDNA expression in Alzheimer’s disease and measurement of a 41-kD protein in cerebrospinal fluid.. J Clin Invest 100, 3093–3104.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moore, A.D., Björklund, A.K., Ekman, D., Bornberg-Bauer, E., and Elofsson, A. (2008). Arrangements in the modular evolution of proteins. Trends Biochem Sci 33, 444–451.

    Article  CAS  PubMed  Google Scholar 

  • Morales, M.E., White, T.B., Streva, V.A., DeFreece, C.B., Hedges, D.J., and Deininger, P.L. (2015). The contribution of alu elements to mutagenic DNA double-strand break repair. PLoS Genet 11, e1005016.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morales-Hernández, A., González-Rico, F.J., Román, A.C., Rico-Leo, E., Alvarez-Barrientos, A., Sánchez, L., Macia, Á., Heras, S.R., García-Pérez, J.L., Merino, J.M., et al. (2016). Alu retrotransposons promote differentiation of human carcinoma cells through the aryl hydrocarbon receptor. Nucleic Acids Res 44, 4665–4683.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moyers, B.A., and Zhang, J. (2016). Evaluating phylostratigraphic evidence for widespread de novo gene birth in genome evolution. Mol Biol Evol 33, 1245–1256.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muller, H.J. (1935). The origination of chromatin deficiencies as minute deletions subject to insertion elsewhere. Genetics 17, 237–252.

    Google Scholar 

  • Nakanishi, A., Kobayashi, N., Suzuki-Hirano, A., Nishihara, H., Sasaki, T., Hirakawa, M., Sumiyama, K., Shimogori, T., and Okada, N. (2012). A SINE-derived element constitutes a unique modular enhancer for mammalian diencephalic Fgf8. PLoS ONE 7, e43785.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nefedova, L.N., Kuzmin, I.V., Makhnovskii, P.A., and Kim, A.I. (2014). Domesticated retroviral GAG gene in Drosophila: new functions for an old gene. Virology 450–451, 196–204.

    Article  CAS  PubMed  Google Scholar 

  • Nei, M. (1969). Gene duplication and nucleotide substitution in evolution. Nature 221, 40–42.

    Article  CAS  PubMed  Google Scholar 

  • Nekrutenko, A., Makova, K.D., and Li, W.H. (2002). The KA/KS ratio test for assessing the protein-coding potential of genomic regions: an empirical and simulation study. Genome Res 12, 198–202.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nelson, A.C., and Wardle, F.C. (2013). Conserved non-coding elements and cis regulation: actions speak louder than words. Development 140, 1385–1395.

    Article  CAS  PubMed  Google Scholar 

  • Neme, R., Amador, C., Yildirim, B., McConnell, E., and Tautz, D. (2017). Random sequences are an abundant source of bioactive RNAs or peptides. Nat ecol evol 1, 0127.

    Article  Google Scholar 

  • Neme, R., and Tautz, D. (2014). Evolution: dynamics of de novo gene emergence. Curr Biol 24, R238–R240.

    Google Scholar 

  • Neme, R., and Tautz, D. (2016). Fast turnover of genome transcription across evolutionary time exposes entire non-coding DNA to de novo gene emergence. eLife 5, e09977.

    PubMed  Google Scholar 

  • Nishihara, H., Kobayashi, N., Kimura-Yoshida, C., Yan, K., Bormuth, O., Ding, Q., Nakanishi, A., Sasaki, T., Hirakawa, M., Sumiyama, K., et al. (2016). Coordinately co-opted multiple transposable elements constitute an enhancer for wnt5a expression in the mammalian secondary palate. PLoS Genet 12, e1006380.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nissimov, J.I., Pagarete, A., Ma, F., Cody, S., Dunigan, D.D., Kimmance, S.A., and Allen, M.J. (2017). Coccolithoviruses: a review of crosskingdom genomic thievery and metabolic thuggery. Viruses 9, pii: E52.

    Google Scholar 

  • Notwell, J.H., Chung, T., Heavner, W., and Bejerano, G. (2015). A family of transposable elements co-opted into developmental enhancers in the mouse neocortex. Nat Commun 6, 6644.

    Article  CAS  PubMed  Google Scholar 

  • Ohno, S. (1970). Evolution by gene duplication (Berlin: Springer Verlag).

    Book  Google Scholar 

  • Ohno, S. (1972). So much “junk” DNA in our genome. Brookhaven Symp Biol 23, 366–370.

    CAS  PubMed  Google Scholar 

  • Ohno, S., Wolf, U., and Atkin, N.B. (1968). Evolution from fish to mammals by gene duplication. Hereditas 59, 169–187.

    Article  CAS  PubMed  Google Scholar 

  • Okada, N., Sasaki, T., Shimogori, T., and Nishihara, H. (2010). Emergence of mammals by emergency: exaptation. Genes Cells 15, 801–812.

    CAS  PubMed  Google Scholar 

  • Orgel, L.E., and Crick, F.H.C. (1980). Selfish DNA: the ultimate parasite. Nature 284, 604–607.

    Article  CAS  PubMed  Google Scholar 

  • Palmer, A.A., and Dulawa, S.C. (2010). Murine warriors or worriers: the saga of Comt1, B2 SINE elements, and the future of translational genetics. Front Neurosci 4, 177.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pandey, R., Bhattacharya, A., Bhardwaj, V., Jha, V., Mandal, A.K., and Mukerji, M. (2016). Alu-miRNA interactions modulate transcript isoform diversity in stress response and reveal signatures of positive selection. Sci Rep 6, 32348.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park, E., and Maquat, L.E. (2013). Staufen-mediated mRNA decay. WIREs RNA 4, 423–435.

    Article  CAS  PubMed  Google Scholar 

  • Pauli, A., Valen, E., and Schier, A.F. (2015). Identifying (non-)coding RNAs and small peptides: challenges and opportunities. BioEssays 37, 103–112.

    Article  CAS  PubMed  Google Scholar 

  • Pei, B., Sisu, C., Frankish, A., Howald, C., Habegger, L., Mu, X.J., Harte, R., Balasubramanian, S., Tanzer, A., Diekhans, M., et al. (2012). The GENCODE pseudogene resource. Genome Biol 13, R51.

    Google Scholar 

  • Peng, L. (2005). Origin and evolution of new exons in the rodent zinc finger protein 39 gene. Chin Sci Bull 50, 1126–1130.

    Article  CAS  Google Scholar 

  • Phillips, P.K., and Heath, J.E. (1992). Heat exchange by the pinna of the african elephant (Loxodonta africana). Comp Biochem Physiol Part A Physiol 101, 693–699.

    Article  CAS  Google Scholar 

  • Piatigorsky, J., and Wistow, G. (1991). The recruitment of crystallins: new functions precede gene duplication. Science 252, 1078–1079.

    Article  CAS  PubMed  Google Scholar 

  • Piya, S., Bennett, M., Rambani, A., and Hewezi, T. (2017). Transcriptional activity of transposable elements may contribute to gene expression changes in the syncytium formed by cyst nematode in arabidopsis roots. Plant Signal Behav 12, e1362521.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Platt, R.N., Vandewege, M.W., and Ray, D.A. (2018). Mammalian transposable elements and their impacts on genome evolution. Chromosome Res 26, 25–43.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Podbevšek, P., Fasolo, F., Bon, C., Cimatti, L., Reißer, S., Carninci, P., Bussi, G., Zucchelli, S., Plavec, J., and Gustincich, S. (2018). Structural determinants of the SINE B2 element embedded in the long non-coding RNA activator of translation AS Uchl1. Sci Rep 8, 3189.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Polesskaya, O., Kananykhina, E., Roy-Engel, A.M., Nazarenko, O., Kulemzina, I., Baranova, A., Vassetsky, Y., and Myakishev-Rempel, M. (2018). The role of Alu-derived RNAs in Alzheimer’s and other neurodegenerative conditions. Med Hypotheses 115, 29–34.

    Article  CAS  PubMed  Google Scholar 

  • Poliseno, L., Salmena, L., Zhang, J., Carver, B., Haveman, W.J., and Pandolfi, P.P. (2010). A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature 465, 1033–1038.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ponicsan, S.L., Kugel, J.F., and Goodrich, J.A. (2010). Genomic gems: SINE RNAs regulate mRNA production. Curr Opin Genets Dev 20, 149–155.

    Article  CAS  Google Scholar 

  • Post, T.W., Arce, M.A., Liszewski, M.K., Thompson, E.S., Atkinson, J.P., and Lublin, D.M. (1990). Structure of the gene for human complement protein decay accelerating factor. J Immunol 144, 740–744.

    CAS  PubMed  Google Scholar 

  • Potrzebowski, L., Vinckenbosch, N., Marques, A.C., Chalmel, F., Jégou, B., and Kaessmann, H. (2008). Chromosomal gene movements reflect the recent origin and biology of therian sex chromosomes. PLoS Biol 6, e80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raj, A., and van Oudenaarden, A. (2008). Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135, 216–226.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ram, O., Schwartz, S., and Ast, G. (2008). Multifactorial interplay controls the splicing profile of Alu-derived exons. Mol Cell Biol 28, 3513–3525.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rayan, N.A., Del Rosario, R.C.H., and Prabhakar, S. (2016). Massive contribution of transposable elements to mammalian regulatory sequences. Sem Cell Dev Biol 57, 51–56.

    Article  CAS  Google Scholar 

  • Rebollo, R., Romanish, M.T., and Mager, D.L. (2012). Transposable elements: an abundant and natural source of regulatory sequences for host genes. Annu Rev Genet 46, 21–42.

    Article  CAS  PubMed  Google Scholar 

  • Rosikiewicz, W., Kabza, M., Kosinski, J.G., Ciomborowska-Basheer, J., Kubiak, M.R., and Makalowska, I. (2017). RetrogeneDB-a database of plant and animal retrocopies. Database (Oxford) 2017.

    Google Scholar 

  • Rohrmoser, M., Kluge, M., Yahia, Y., Gruber-Eber, A., Maqbool, M.A., Forné, I., Krebs, S., Blum, H., Greifenberg, A.K., Geyer, M., et al. (2018). MIR sequences recruit zinc finger protein ZNF768 to expressed genes. Nucleic Acids Res 107.

    Google Scholar 

  • Rote, N.S., Chakrabarti, S., and Stetzer, B.P. (2004). The role of human endogenous retroviruses in trophoblast differentiation and placental development. Placenta 25, 673–683.

    Article  CAS  PubMed  Google Scholar 

  • Sasaki, T., Nishihara, H., Hirakawa, M., Fujimura, K., Tanaka, M., Kokubo, N., Kimura-Yoshida, C., Matsuo, I., Sumiyama, K., Saitou, N., et al. (2008). Possible involvement of SINEs in mammalian-specific brain formation. Proc Natl Acad Sci USA 105, 4220–4225.

    Article  PubMed  PubMed Central  Google Scholar 

  • Schmitz, J. (2012). SINEs as driving forces in genome evolution. Genome Dyn 7, 92–107.

    Article  CAS  PubMed  Google Scholar 

  • Schmitz, J., and Brosius, J. (2011). Exonization of transposed elements: A challenge and opportunity for evolution. Biochimie 93, 1928–1934.

    Article  CAS  PubMed  Google Scholar 

  • Schmitz, J.F., and Bornberg-Bauer, E. (2017). Fact or fiction: updates on how protein-coding genes might emerge de novo from previously noncoding DNA. F1000Res 6, 57.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sieber, K.B., Bromley, R.E., and Dunning Hotopp, J.C. (2017). Lateral gene transfer between prokaryotes and eukaryotes. Exp Cell Res 358, 421–426.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simonson, T.S., Yang, Y., Huff, C.D., Yun, H., Qin, G., Witherspoon, D.J., Bai, Z., Lorenzo, F.R., Xing, J., Jorde, L.B., et al. (2010). Genetic evidence for high-altitude adaptation in Tibet. Science 329, 72–75.

    Article  CAS  PubMed  Google Scholar 

  • Simonti, C.N., Pavlicev, M., and Capra, J.A. (2017). Transposable element exaptation into regulatory regions is rare, influenced by evolutionary age, and subject to pleiotropic constraints. Mol Biol Evol 34, 2856–2869.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singer, S.S., Männel, D.N., Hehlgans, T., Brosius, J., and Schmitz, J. (2004). From “junk” to gene: curriculum vitae of a primate receptor isoform gene. J Mol Biol 341, 883–886.

    Article  CAS  PubMed  Google Scholar 

  • Smalheiser, N.R., and Torvik, V.I. (2006). Alu elements within human mRNAs are probable microRNA targets. Trends Genets 22, 532–536.

    Article  CAS  Google Scholar 

  • Smith, H.M., and James, L.F. (1958). The taxonomic significance of cloacal bursae in turtles. Trans Kansas Acad Sci 61, 86–96.

    Article  Google Scholar 

  • Soares, M.B., Schon, E., Henderson, A., Karathanasis, S.K., Cate, R., Zeitlin, S., Chirgwin, J., and Efstratiadis, A. (1985). RNA-mediated gene duplication: the rat preproinsulin I gene is a functional retroposon.. Mol Cell Biol 5, 2090–2103.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song, X., and Cao, X. (2017). Transposon-mediated epigenetic regulation contributes to phenotypic diversity and environmental adaptation in rice. Curr Opin Plant Biol 36, 111–118.

    Article  CAS  PubMed  Google Scholar 

  • Sorek, R., Ast, G., and Graur, D. (2002). Alu-containing exons are alternatively spliced. Genome Res 12, 1060–1067.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sorek, R., Lev-Maor, G., Reznik, M., Dagan, T., Belinky, F., Graur, D., and Ast, G. (2004). Minimal conditions for exonization of intronic sequences. Mol Cell 14, 221–231.

    Article  CAS  PubMed  Google Scholar 

  • Stephens, S.G. (1951). Possible significances of duplication in evolution. Adv Genet 4, 247–265.

    Article  CAS  PubMed  Google Scholar 

  • Storz, J.F., and Moriyama, H. (2008). Mechanisms of hemoglobin adaptation to high altitude hypoxia. High Altitude Med Biol 9, 148–157.

    Article  CAS  Google Scholar 

  • Struhl, K. (2007). Transcriptional noise and the fidelity of initiation by RNA polymerase II. Nat Struct Mol Biol 14, 103–105.

    Article  CAS  PubMed  Google Scholar 

  • Su, M., Han, D., Boyd-Kirkup, J., Yu, X., and Han, J.D.J. (2014). Evolution of Alu elements toward enhancers. Cell Rep 7, 376–385.

    Article  CAS  PubMed  Google Scholar 

  • Sundaram, V., Cheng, Y., Ma, Z., Li, D., Xing, X., Edge, P., Snyder, M.P., and Wang, T. (2014). Widespread contribution of transposable elements to the innovation of gene regulatory networks. Genome Res 24, 1963–1976.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sundaram, V., and Wang, T. (2018). Transposable element mediated innovation in gene regulatory landscapes of cells: re-visiting the “genebattery” model. Bioessays 40.

    Google Scholar 

  • Tait, L. (1879). The use of tails. Nature, 603.

    Google Scholar 

  • Tajaddod, M., Tanzer, A., Licht, K., Wolfinger, M.T., Badelt, S., Huber, F., Pusch, O., Schopoff, S., Janisiw, M., Hofacker, I., et al. (2016). Transcriptome-wide effects of inverted SINEs on gene expression and their impact on RNA polymerase II activity. Genome Biol 17, 220.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tashiro, K., Teissier, A., Kobayashi, N., Nakanishi, A., Sasaki, T., Yan, K., Tarabykin, V., Vigier, L., Sumiyama, K., Hirakawa, M., et al. (2011). A mammalian conserved element derived from SINE displays enhancer properties recapitulating Satb2 expression in early-born callosal projection neurons. PLoS ONE 6, e28497.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tattersall, I. (2010). Human evolution and cognition. Theor Biosci 129, 193–201.

    Article  Google Scholar 

  • Tautz, D. (2014). The discovery of de novo gene evolution. Perspect Biol Med 57, 149–161.

    Article  PubMed  Google Scholar 

  • Tautz, D., and Domazet-Lošo, T. (2011). The evolutionary origin of orphan genes. Nat Rev Genet 12, 692–702.

    Article  CAS  PubMed  Google Scholar 

  • Tiedge, H., Chen, W., and Brosius, J. (1993). Primary structure, neuralspecific expression, and dendritic location of human BC200 RNA. J Neurosci 13, 2382–2390.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tiedge, H., Fremeau Jr., R.T., Weinstock, P.H., Arancio, O., and Brosius, J. (1991). Dendritic location of neural BC1 RNA. Proc Natl Acad Sci USA 88, 2093–2097.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Touchon, M., Moura de Sousa, J.A., and Rocha, E.P. (2017). Embracing the enemy: the diversification of microbial gene repertoires by phagemediated horizontal gene transfer. Curr Opin Microbiol 38, 66–73.

    Article  CAS  PubMed  Google Scholar 

  • Trizzino, M., Kapusta, A., and Brown, C.D. (2018). Transposable elements generate regulatory novelty in a tissue-specific fashion. BMC Genomics 19, 468.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trizzino, M., Park, Y.S., Holsbach-Beltrame, M., Aracena, K., Mika, K., Caliskan, M., Perry, G.H., Lynch, V.J., and Brown, C.D. (2017). Transposable elements are the primary source of novelty in primate gene regulation. Genome Res 27, 1623–1633.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ulbricht, R.J., and Emeson, R.B. (2014). One hundred million adenosineto-inosine RNA editing sites: hearing through the noise. Bioessays 36, 730–735.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ulitsky, I., and Bartel, D.P. (2013). lincRNAs: genomics, evolution, and mechanisms. Cell 154, 26–46.

    CAS  PubMed  Google Scholar 

  • van de Lagemaat, L.N., Landry, J.R., Mager, D.L., and Medstrand, P. (2003). Transposable elements in mammals promote regulatory variation and diversification of genes with specialized functions. Trends Genets 19, 530–536

    Article  CAS  Google Scholar 

  • VanKuren, N.W., and Long, M. (2018). Gene duplicates resolving sexual conflict rapidly evolved essential gametogenesis functions. Nat Ecol Evol 2, 705–712.

    Article  PubMed  PubMed Central  Google Scholar 

  • Volff, J.N. (2005). Retrotransposable elements and genome evolution (Basel: S. Karger).

    Book  Google Scholar 

  • Volff, J.N., and Brosius, J. (2007). Modern genomes with retro-look: retrotransposed elements, retroposition and the origin of new genes. Genome Dyn 3, 175–190.

    Article  CAS  PubMed  Google Scholar 

  • Vos, M., Hesselman, M.C., Te Beek, T.A., van Passel, M.W.J., and Eyre-Walker, A. (2015). Rates of lateral gene transfer in prokaryotes: high but why? Trends Microbiol 23, 598–605.

    Article  CAS  PubMed  Google Scholar 

  • Wade, J.T., and Grainger, D.C. (2018). Spurious transcription and its impact on cell function. Transcription 9, 182–189.

    Article  CAS  PubMed  Google Scholar 

  • Wallace, A.R. (1889). Darwinism, 1st edn (London: Macmillan).

    Google Scholar 

  • Wallace, M.R., Andersen, L.B., Saulino, A.M., Gregory, P.E., Glover, T.W., and Collins, F.S. (1991). A de novo Alu insertion results in neurofibromatosis type 1. Nature 353, 864–866.

    Article  CAS  PubMed  Google Scholar 

  • Wang, C., and Huang, S. (2014). Nuclear function of Alus. Nucleus 5, 131–137.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, H., Iacoangeli, A., Lin, D., Williams, K., Denman, R.B., Hellen, C. U.T., and Tiedge, H. (2005). Dendritic BC1 RNA in translational control mechanisms. J Cell Biol 171, 811–821.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, H., and Tiedge, H. (2004). Translational control at the synapse. Neuroscientist 10, 456–466.

    Article  CAS  PubMed  Google Scholar 

  • Wang, J., Gong, C., and Maquat, L.E. (2013). Control of myogenesis by rodent SINE-containing lncRNAs. Genes Dev 27, 793–804.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, J., Vicente-García, C., Seruggia, D., Moltó, E., Fernandez-Miñán, A., Neto, A., Lee, E., Gómez-Skarmeta, J.L., Montoliu, L., Lunyak, V. V., et al. (2015). MIR retrotransposon sequences provide insulators to the human genome. Proc Natl Acad Sci USA 112, e4428–E4437.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, L., and Jordan, I.K. (2018). Transposable element activity, genome regulation and human health. Curr Opin Genets Dev 49, 25–33.

    Article  CAS  Google Scholar 

  • Wang, T., Zeng, J., Lowe, C.B., Sellers, R.G., Salama, S.R., Yang, M., Burgess, S.M., Brachmann, R.K., and Haussler, D. (2007). Speciesspecific endogenous retroviruses shape the transcriptional network of the human tumor suppressor protein p53. Proc Natl Acad Sci USA 104, 18613–18618.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, W., Brunet, F.G., Nevo, E., and Long, M. (2002). Origin of sphinx, a young chimeric RNA gene in Drosophila melanogaster. Proc Natl Acad Sci USA 99, 4448–4453.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson, B.A., and Masel, J. (2011). Putatively noncoding transcripts show extensive association with ribosomes. Genome Biol Evol 3, 1245–1252.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wistow, G. (1993). Lens crystallins: gene recruitment and evolutionary dynamism. Trends Biochem Sci 18, 301–306.

    Article  CAS  PubMed  Google Scholar 

  • Wu, T., and Kayser, B. (2006). High altitude adaptation in Tibetans. High Altitude Med Biol 7, 193–208.

    Article  Google Scholar 

  • Xiao, W., Liu, H., Li, Y., Li, X., Xu, C., Long, M., and Wang, S. (2009). A rice gene of de novo origin negatively regulates pathogen-induced defense response. PLoS ONE 4, e4603.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie, M., Hong, C., Zhang, B., Lowdon, R.F., Xing, X., Li, D., Zhou, X., Lee, H.J., Maire, C.L., Ligon, K.L., et al. (2013). DNA hypomethylation within specific transposable element families associates with tissue-specific enhancer landscape. Nat Genet 45, 836–841.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang, S., Arguello, J.R., Li, X., Ding, Y., Zhou, Q., Chen, Y., Zhang, Y., Zhao, R., Brunet, F., Peng, L., et al. (2008). Repetitive elementmediated recombination as a mechanism for new gene origination in Drosophila. PLoS Genet 4, e3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu, H., Jiang, H., Zhou, Q., Yang, J., Cun, Y., Su, B., Xiao, C., and Wang, W. (2006). Origination and evolution of a human-specific transmembrane protein gene, c1orf37-dup. Hum Mol Genets 15, 1870–1875.

    Article  CAS  Google Scholar 

  • Yu, H., Zhao, X., Su, B., Li, D., Xu, Y., Luo, S., Xiao, C., and Wang, W. (2005). Expression of NF1 pseudogenes. Hum Mutat 26, 487–488.

    Article  CAS  PubMed  Google Scholar 

  • Zeng, L., Pederson, S.M., Cao, D., Qu, Z., Hu, Z., Adelson, D.L., and Wei, C. (2018a). Genome-wide analysis of the association of transposable elements with gene regulation suggests that Alu elements have the largest overall regulatory impact. J Comput Biol 25, 551–562.

    Article  CAS  PubMed  Google Scholar 

  • Zeng, L., Pederson, S.M., Kortschak, R.D., and Adelson, D.L. (2018b). Transposable elements and gene expression during the evolution of amniotes. Mobile DNA 9, 17.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang, W., Landback, P., Gschwend, A.R., Shen, B., and Long, M. (2015). New genes drive the evolution of gene interaction networks in the human and mouse genomes. Genome Biol 16, 202.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, Y., Lu, S., Zhao, S., Zheng, X., Long, M., and Wei, L. (2009). Positive selection for the male functionality of a co-retroposed gene in the hominoids. BMC Evol Biol 9, 252.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, Y.E., Landback, P., Vibranovski, M., and Long, M. (2012). New genes expressed in human brains: implications for annotating evolving genomes. Bioessays 34, 982–991.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, Y.E., Landback, P., Vibranovski, M.D., and Long, M.Y. (2011). Accelerated recruitment of new brain development genes into the human genome. PLoS Biol 9, e1001179.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, Y.E., and Long, M. (2014). New genes contribute to genetic and phenotypic novelties in human evolution. Curr Opin Genets Dev 29, 90–96.

    Article  CAS  Google Scholar 

  • Zhang, Z., Harrison, P.M., Liu, Y., and Gerstein, M. (2003). Millions of years of evolution preserved: a comprehensive catalog of the processed pseudogenes in the human genome. Genome Res 13, 2541–2558.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao, D., Ferguson, A.A., and Jiang, N. (2016). What makes up plant genomes: The vanishing line between transposable elements and genes. Biochim Biophys Acta Gene Regul Mech 1859, 366–380.

    Article  CAS  Google Scholar 

  • Zucchelli, S., Patrucco, L., Persichetti, F., Gustincich, S., and Cotella, D. (2016). Engineering translation in mammalian cell factories to increase protein yield: the unexpected use of long non-coding SINEUP RNAs. Comput Struct Biotech J 14, 404–410.

    Article  CAS  Google Scholar 

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Acknowledgements

Apologies to those whose articles were not cited which, in part, is owed to the explosive growth of the literature in the field. The author is grateful to Stephanie Klco-Brosius for a last minute review of language.

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Brosius, J. Exaptation at the molecular genetic level. Sci. China Life Sci. 62, 437–452 (2019). https://doi.org/10.1007/s11427-018-9447-8

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