Cooperation and Competition in Mammalian Evolution

Gene Domestication from LTR Retrotransposons
  • Tomoko Kaneko-Ishino
  • Fumitoshi IshinoEmail author


Mammalian genomes have had to endure the integration of exogenous DNA sequences over the course of time. In most cases, such events have proven harmful to individuals thus afflicted, but in the long-term gene domestication of exogenous DNA sequences, such as LTR retrotransposons, has also served as a driving mechanism in biological evolution. This is especially the case in eutherian mammals, in which two lines of domesticated genes increased in number in a common eutherian ancestor, eleven sushi-ichi-related retrotransposon homologs (SIRH)/retrotransposon Gag-like (RTL) genes and more than fifteen paraneoplastic Ma antigen (PNMA) genes. It is clear that these SIRH/RTL and PNMA genes were positively selected due to the advantage conferred on eutherian reproductive success. Thus, the principle of “competition among individuals within the same species” in the Darwinian theory of evolution is effectively at work in the domestication process. However, when the number of domestication events is taken into account, how could the common eutherian ancestor have acquired that many domesticated genes? We suggest that sexual mating across multiple generations of individuals with one or a small number of such domesticated genes may have been critically important for accumulating all of them into a single line, thus leading to the common eutherian ancestor. Then, we would like to propose that “cooperation among individuals within the same species” in the form of interactive behaviors of the individuals within a tightly delimited species is also at work in this process.


  1. Agrawal A, Eastman QM, Schatz DG (1998) Transposition mediated by RAG1 and RAG2 and its implications for the evolution of the immune system. Nature 394:744–751CrossRefGoogle Scholar
  2. Barlow DP (1993) Methylation and imprinting: from host defense to gene regulation? Science 260:309–310CrossRefGoogle Scholar
  3. Belshaw R, Dawson AL, Woolven-Allen J, Redding J, Burt A, Tristem M (2005) Genomewide screening reveals high levels of insertional polymorphism in the human endogenous retrovirus family HERV-K(HML2): implications for present-day activity. J Virol 79:12507–12514CrossRefGoogle Scholar
  4. Belyi VA, Levine AJ, Skalka AM (2010) Unexpected inheritance: multiple integrations of ancient bornavirus and ebolavirus/marburgvirus sequences in vertebrate genomes. PLoS Pathog 6:e1001030CrossRefGoogle Scholar
  5. Bernard D, Méhul B, Thomas-Collignon A, Delattre C, Donovan M, Schmidt R (2005) Identification and characterization of a novel retroviral-like aspartic protease specifically expressed in human epidermis. J Invest Dermatol 125:278–287CrossRefGoogle Scholar
  6. Blond J-L, Lavillette D, Cheynet V, Bouton O, Oriol G, Chapel-Fernandes S, Mandrand B, Mallet F, Cosset FL (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 74:3321–3329CrossRefGoogle Scholar
  7. Brandt J, Schrauth S, Veith AM, Froschauer A, Haneke T, Schultheis C, Gessler M, Leimeister C, Volff JN (2005) Transposable elements as a source of genetic innovation: expression and evolution of a family of retrotransposon-derived neogenes in mammals. Gene 345:101–111CrossRefGoogle Scholar
  8. Brosius J (1999) RNAs from all categories generate retrosequences that may be exapted as novel genes or regulatory elements. Gene 238:115–134CrossRefGoogle Scholar
  9. Brosius J, Gould SJ (1992) On “genomenclature”: a comprehensive (and respectful) taxonomy for pseudogenes and other “junk DNA”. Proc Natl Acad Sci USA 89:10706–10710CrossRefGoogle Scholar
  10. Campillos M, Doerks T, Shah PK, Bork P (2006) Computational characterization of multiple Gag-like human proteins. Trends Genet 22:585–589CrossRefGoogle Scholar
  11. Charlier C, Segers K, Wagenaar D, Karim L, Berghmans S, Jaillon O, Shay T, Weissenbach J, Cockett N, Gyapay G, Georges M (2001) Human-ovine comparative sequencing of a 250-kb imprinted domain encompassing the callipyge (clpg) locus and identification of six imprinted transcripts: DLK1, DAT, GTL2, PEG11, antiPEG11, and MEG8. Genome Res 11:850–862CrossRefGoogle Scholar
  12. Cho G, Bhat SS, Gao J, Collins JS, Rogers RC, Simensen RJ, Schwartz CE, Golden JA, Srivastava AK (2008a) Evidence that SIZN1 is a candidate X-linked mental retardation gene. Am J Med Genet A 146A:2644–2650CrossRefGoogle Scholar
  13. Cho G, Lim Y, Zand D, Golden JA (2008b) Sizn1 is a novel protein that functions as a transcriptional coactivator of bone morphogenic protein signaling. Mol Cell Biol 28:1565–1572CrossRefGoogle Scholar
  14. Cho G, Lim Y, Golden JA (2011) XLMR candidate mouse gene, Zcchc12 (Sizn1) is a novel marker of Cajal-Retzius cells. Gene Expr Patterns 11:216–220CrossRefGoogle Scholar
  15. Clark MB, Jänicke M, Gottesbühren U, Kleffmann T, Legge M, Poole ES, Tate WP (2007) Mammalian gene PEG10 expresses two reading frames by high efficiency −1 frameshifting in embryonic-associated tissues. J Biol Chem 282:37359–37369CrossRefGoogle Scholar
  16. Dupressoir A, Marceau G, Vernochet C, Bénit L, Kanellopoulos C, Sapin V, Heidmann T (2005) Syncytin-A and syncytin-B, two fusogenic placenta-specific murine envelope genes of retroviral origin conserved in Muridae. Proc Natl Acad Sci USA 102:725–730CrossRefGoogle Scholar
  17. Edwards CA, Mungall AJ, Matthews L, Ryder E, Gray DJ, Pask AJ, Shaw G, Graves JA, Rogers J, SAVOIR Consortium, Dunham I, Renfree MB, Ferguson-Smith AC (2008) The evolution of the DLK1-DIO3 imprinted domain in mammals. PLoS Biol 6:e135CrossRefGoogle Scholar
  18. Gould SJ, Vrba ES (1982) Exaptation; a missing term in the science of form. Paleobiology 8:4–15CrossRefGoogle Scholar
  19. Gu X, Wang Y, Gu J (2002) Age distribution of human gene families shows significant roles of both large- and small-scale duplications in vertebrate evolution. Nat Genet 31:205–209CrossRefGoogle Scholar
  20. Hanson D, Murray PG, O’Sullivan J, Urquhart J, Daly S, Bhaskar SS, Biesecker LG, Skae M, Smith C, Cole T, Kirk J, Chandler K, Kingston H, Donnai D, Clayton PE, Black GC (2011a) Exome sequencing identifies CCDC8 mutations in 3-M syndrome, suggesting that CCDC8 contributes in a pathway with CUL7 and OBSL1 to control human growth. Am J Hum Genet 89:148–153CrossRefGoogle Scholar
  21. Hanson D, Murray PG, Black GC, Clayton PE (2011b) The genetics of 3-m syndrome: unravelling a potential new regulatory growth pathway. Horm Res Paediatr 76:369–378CrossRefGoogle Scholar
  22. Heidmann O, Vernochet C, Dupressoir A, Heidmann T (2009) Identification of an endogenous retroviral envelope gene with fusogenic activity and placenta-specific expression in the rabbit: a new “syncytin” in a third order of mammals. Retrovirology 6:107CrossRefGoogle Scholar
  23. Hiom K, Mele M, Gellert M (1998) DNA transposition by the RAG1 and RAG2 proteins: a possible source of oncogenic translocations. Cell 94:463–470CrossRefGoogle Scholar
  24. Horie M, Honda T, Suzuki Y, Kobayashi Y, Daito T, Oshida T, Ikuta K, Jern P, Gojobori T, Coffin JM, Tomonaga K (2010) Endogenous non-retroviral RNA virus elements in mammalian genomes. Nature 463:84–87CrossRefGoogle Scholar
  25. Hudson ME, Lisch DR, Quail PH (2003) The FHY3 and FAR1 genes encode transposase-related proteins involved in regulation of gene expression by the phytochrome A-signaling pathway. Plant J 34:453–471CrossRefGoogle Scholar
  26. Irie M, Yoshikawa M, Ono R, Iwafune H, Furuse T, Yamada I, Wakana S, Yamashita Y, Abe T, Ishino F, Kaneko-Ishino T (2015) Cognitive function related to the Sirh11/Zcchc16 gene acquired from an LTR retrotransposon in eutherians. PLoS Genet 11:e1005521CrossRefGoogle Scholar
  27. Irie M, Koga A, Kaneko-Ishino T, Ishino F (2016) An LTR retrotransposon-derived gene displays lineage-specific structural and putative species-specific functional variations in eutherians. Front Chem 4:26CrossRefGoogle Scholar
  28. Irie M, Ito J, Furuse T, Ishida S, Yamada I, Wakana S, Kiyonari H, Kihara M, Tachibana S, Kohda T, Tanaka, K Ishino F, Kaneko-Ishino T (submitted) Gene targeting of an LTR retrotransposon-derived Sirh3/Rtl6 gene leads to a prolonged sleep phenotype in miceGoogle Scholar
  29. Iwasaki S, Suzuki S, Clark H, Ono R, Shaw G, Renfree MB, Kaneko-Ishino T, Ishino F (2013) Identification of novel PNMA-MS1 in marsupials suggests LTR retrotransposon-derived PNMA genes differently expanded in marsupials and eutherians. DNA Res 20:425–436CrossRefGoogle Scholar
  30. Kaneko-Ishino T, Ishino F (2010) Retrotransposon silencing by DNA methylation contributed to the evolution of placentation and genomic imprinting in mammals. Dev Growth Differ 52:533–543CrossRefGoogle Scholar
  31. Kaneko-Ishino T, Ishino F (2012) The role of genes domesticated from LTR retrotransposons and retroviruses in mammals. Front Microbiol 3:262CrossRefGoogle Scholar
  32. Kaneko-Ishino T, Ishino F (2015) Mammalian-specific genomic functions: newly acquired traits generated by genomic imprinting and LTR retrotransposon-derived genes in mammals. Proc Jpn Acad Ser B Phys Biol Sci 91:511–538CrossRefGoogle Scholar
  33. Kaneko-Ishino T, Ishino F (2019) Evolution of viviparity in mammals: what genomic imprinting tells us about mammalian placental evolution. Reprod Fert Dev. Scholar
  34. Kaneko-Ishino T, Irie M, Ishino F (2017) Mammalian-specific traits generated by LTR retrotransposon-drived genes. In: Pontarotti P (ed) Evolutionary biology: self/nonself evolution, species and complex traits evolution, methods and concepts. Springer International Publishing, pp 129–145Google Scholar
  35. Kitazawa M, Tamura M, Kaneko-Ishino T, Ishino F (2017) Severe damage to the placental fetal capillary network causes mid to late fetal lethality and reduction of placental size in Peg11/Rtl1 KO mice. Genes Cells 22:174–188CrossRefGoogle Scholar
  36. Kokosar J, Kordiš D (2013) Genesis and regulatory wiring of retroelement-derived domesticated genes: a phylogenomic perspective. Mol Biol Evol 30:1015–1031CrossRefGoogle Scholar
  37. Kordiš D (2017) The life history of domesticated genes illuminates the evolution of novel mammalian genes. In: Pontarotti P (ed) Evolutionary biology: self/nonself evolution, species and complex traits evolution, methods and concepts. Springer International Publishing, pp 129–145Google Scholar
  38. Lin R, Ding L, Casola C, Ripoll DR, Feschotte C, Wang H (2007) Transposase-derived transcription factors regulate light signaling in Arabidopsis. Science 318:1302–1305CrossRefGoogle Scholar
  39. Lisch DR, Freeling M, Langham RJ, Choy MY (2001) Mutator transposase is widespread in the grasses. Plant Physiol 125:1293–1303CrossRefGoogle Scholar
  40. Malik HS, Henikoff S, Eickbush TH (2000) Poised for contagion: evolutionary origins of the infectious abilities of invertebrate retroviruses. Genome Res 10:1307–1318CrossRefGoogle Scholar
  41. Manktelow E, Shigemoto K, Brierley I (2005) Characterization of the frameshift signal of Edr, a mammalian example of programmed −1 ribosomal frameshifting. Nucleic Acids Res 33:1553–1563CrossRefGoogle Scholar
  42. Matsui T, Kinoshita-Ida Y, Hayashi-Kisumi F, Hata M, Matsubara K, Chiba M, Katahira-Tayama S, Morita K, Miyachi Y, Tsukita S (2006) Mouse homologue of skin-specific retroviral-like aspartic protease involved in wrinkle formation. J Biol Chem 281:27512–27525CrossRefGoogle Scholar
  43. Matsui T, Miyamoto K, Kubo A, Kawasaki H, Ebihara T, Hata K, Tanahashi S, Ichinose S, Imoto I, Inazawa J, Kudoh J, Amagai M (2011) SASPase regulates stratum corneum hydration through profilaggrin-to-filaggrin processing. EMBO Mol Med 3:320–333CrossRefGoogle Scholar
  44. Mi S, Lee X, Li X-P, Veldman GM, Finnerty H, Racie L, LaVallie E, Tang X-Y, Edouard P, Howes S, Keith JC Jr, McCoy JM (2000) Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403:785–789CrossRefGoogle Scholar
  45. Nagasaki K, Manabe T, Hanzawa H, Maass N, Tsukada T, Yamaguchi K (1999) Identification of a novel gene, LDOC1, down-regulated in cancer cell lines. Cancer Lett 140:227–234CrossRefGoogle Scholar
  46. Nakamura TM, Cech TR (1998) Reversing time: origin of telomerase. Cell 92:587–590CrossRefGoogle Scholar
  47. Naruse M, Ono R, Irie M, Nakamura K, Furuse T, Hino T, Oda K, Kashimura M, Yamada I, Wakana S, Yokoyama M, Ishino F, Kaneko-Ishino T (2014) Sirh7/Ldoc1 knockout mice exhibit placental P4 overproduction and delayed parturition. Development 141:4763–4771CrossRefGoogle Scholar
  48. Naville M, Warren IA, Haftek-Terreau Z, Chalopin D, Brunet F, Levin P, Galiana D, Volff JN (2016) Not so bad after all: retroviruses and long terminal repeat retrotransposons as a source of new genes in vertebrates. Clin Microbiol Infect 22:312–323CrossRefGoogle Scholar
  49. 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:R74CrossRefGoogle Scholar
  50. Ono R, Kobayashi S, Wagatsuma H, Aisaka K, Kohda T, Kaneko-Ishino T, Ishino F (2001) A retrotransposon-derived gene, PEG10, is a novel imprinted gene located on human chromosome 7q21. Genomics 73:232–237CrossRefGoogle Scholar
  51. Ono R, Nakamura K, Inoue K, Naruse M, Usami T, Wakisaka-Saito N, Hino T, Suzuki-Migishima R, Ogonuki N, Miki H, Kohda T, Ogura A, Yokoyama M, Kaneko-Ishino T, Ishino F (2006) Deletion of PEG10, an imprinted gene acquired from a retrotransposon, causes early embryonic lethality. Nat Genet 38:101–106CrossRefGoogle Scholar
  52. Ono R, Kuroki Y, Naruse M, Ishii M, Iwasaki S, Toyoda A, Fujiyama A, Shaw G, Renfree MB, Kaneko-Ishino T and Ishino F (2011) Identification of tammar wallaby SIRH12, derived from a marsupial-specific retrotransposition event. DNA Res 18:211–219CrossRefGoogle Scholar
  53. Pavlícek A, Paces J, Elleder D, Hejnar J (2002) Processed pseudogenes of human endogenous retroviruses generated by LINEs: their integration, stability, and distribution. Genome Res 12:391–399CrossRefGoogle Scholar
  54. Renfree MB (2010) Marsupials: placental mammals with a difference. Placenta 31(Suppl):S21–S26CrossRefGoogle Scholar
  55. Renfree MB, Suzuki S, Kaneko-Ishino T (2013) The origin and evolution of genomic imprinting and viviparity in mammals. Philos Trans R Soc Lond B Biol Sci 368:20120151CrossRefGoogle Scholar
  56. Ribet D, Harper F, Dupressoir A, Dewannieux M, Pierron G, Heidmann T (2008) An infectious progenitor for the murine IAP retrotransposon: emergence of an intracellular genetic parasite from an ancient retrovirus. Genome Res 18:597–609CrossRefGoogle Scholar
  57. Schüller M, Jenne D and Voltz R (2005) The human PNMA family: novel neuronal proteins implicated in paraneoplastic neurological disease. J Neuroimmunol 169:172–176CrossRefGoogle Scholar
  58. Sekita Y, Wagatsuma H, Nakamura K, Ono R, Kagami M, Wakisaka N, Hino T, Suzuki-Migishima R, Kohda T, Ogura A, Ogata T, Yokoyama M, Kaneko-Ishino T, Ishino F (2008) Role of retrotransposon-derived imprinted gene, Rtl1, in the feto-maternal interface of mouse placenta. Nat Genet 40:243–248CrossRefGoogle Scholar
  59. Shigemoto K, Brennan J, Walls E, Watson CJ, Stott D, Rigby PW, Reith AD (2001) Identification and characterisation of a developmentally regulated mammalian gene that utilises-1 programmed ribosomal frameshifting. Nucleic Acids Res 29:4079–4088CrossRefGoogle Scholar
  60. Suga H, Koyanagi M, Hoshiyama D, Ono K, Iwabe N, Kuma K, Miyata T (1999) Extensive gene duplication in the early evolution of animals before the parazoan-eumetazoan split demonstrated by G proteins and protein tyrosine kinases from sponge and hydra. Mol Evol 48:646–653CrossRefGoogle Scholar
  61. Suzuki S, Ono R, Narita T, Pask AJ, Shaw G, Wang C, Kohda T, Alsop AE, Graves MJA, Kohara Y, Ishino F, Renfree MB, Kaneko-Ishino T (2007) Retrotransposon silencing by DNA methylation can drive mammalian genomic imprinting. PLoS Genet 3:e55CrossRefGoogle Scholar
  62. Vanin EF (1985) Processed pseudogenes: characteristics and evolution. Annu Rev Genet 19:253–272CrossRefGoogle Scholar
  63. Youngson NA, Kocialkowski S, Peel N, Ferguson-Smith AC (2005) A small family of sushi-class retrotransposon-derived genes in mammals and their relation to genomic imprinting. J Mol Evol 61:481–490CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Tokai UniversityIsehara CityJapan
  2. 2.Tokyo Medical and Dental UniversityTokyoJapan

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