Skip to main content

Cooperation and Competition in Mammalian Evolution

Gene Domestication from LTR Retrotransposons

  • Chapter
  • First Online:
Evolution, Origin of Life, Concepts and Methods

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Agrawal A, Eastman QM, Schatz DG (1998) Transposition mediated by RAG1 and RAG2 and its implications for the evolution of the immune system. Nature 394:744–751

    Article  CAS  Google Scholar 

  • Barlow DP (1993) Methylation and imprinting: from host defense to gene regulation? Science 260:309–310

    Article  CAS  Google Scholar 

  • 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 79:12507–12514

    Article  CAS  Google Scholar 

  • Belyi VA, Levine AJ, Skalka AM (2010) Unexpected inheritance: multiple integrations of ancient bornavirus and ebolavirus/marburgvirus sequences in vertebrate genomes. PLoS Pathog 6:e1001030

    Article  Google Scholar 

  • 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 125:278–287

    Article  CAS  Google Scholar 

  • 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 74:3321–3329

    Article  CAS  Google Scholar 

  • 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 345:101–111

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Campillos M, Doerks T, Shah PK, Bork P (2006) Computational characterization of multiple Gag-like human proteins. Trends Genet 22:585–589

    Article  CAS  Google Scholar 

  • 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 11:850–862

    Article  CAS  Google Scholar 

  • 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:2644–2650

    Article  CAS  Google Scholar 

  • 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 28:1565–1572

    Article  CAS  Google Scholar 

  • Cho G, Lim Y, Golden JA (2011) XLMR candidate mouse gene, Zcchc12 (Sizn1) is a novel marker of Cajal-Retzius cells. Gene Expr Patterns 11:216–220

    Article  CAS  Google Scholar 

  • 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 282:37359–37369

    Article  CAS  Google Scholar 

  • 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 102:725–730

    Article  CAS  Google Scholar 

  • 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:e135

    Article  Google Scholar 

  • Gould SJ, Vrba ES (1982) Exaptation; a missing term in the science of form. Paleobiology 8:4–15

    Article  Google Scholar 

  • 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 31:205–209

    Article  CAS  Google Scholar 

  • 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 89:148–153

    Article  CAS  Google Scholar 

  • 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 76:369–378

    Article  CAS  Google Scholar 

  • 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 6:107

    Article  Google Scholar 

  • Hiom K, Mele M, Gellert M (1998) DNA transposition by the RAG1 and RAG2 proteins: a possible source of oncogenic translocations. Cell 94:463–470

    Article  CAS  Google Scholar 

  • 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 463:84–87

    Article  CAS  Google Scholar 

  • 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 34:453–471

    Article  CAS  Google Scholar 

  • 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:e1005521

    Article  Google Scholar 

  • 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 4:26

    Article  Google Scholar 

  • 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 mice

    Google Scholar 

  • 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 20:425–436

    Article  CAS  Google Scholar 

  • 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 52:533–543

    Article  CAS  Google Scholar 

  • Kaneko-Ishino T, Ishino F (2012) The role of genes domesticated from LTR retrotransposons and retroviruses in mammals. Front Microbiol 3:262

    Article  CAS  Google Scholar 

  • 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 91:511–538

    Article  CAS  Google Scholar 

  • Kaneko-Ishino T, Ishino F (2019) Evolution of viviparity in mammals: what genomic imprinting tells us about mammalian placental evolution. Reprod Fert Dev. https://doi.org/10.1071/RD18127

    Article  Google Scholar 

  • 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 129–145

    Google Scholar 

  • 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 22:174–188

    Article  CAS  Google Scholar 

  • Kokosar J, Kordiš D (2013) Genesis and regulatory wiring of retroelement-derived domesticated genes: a phylogenomic perspective. Mol Biol Evol 30:1015–1031

    Article  CAS  Google Scholar 

  • 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 129–145

    Google Scholar 

  • Lin R, Ding L, Casola C, Ripoll DR, Feschotte C, Wang H (2007) Transposase-derived transcription factors regulate light signaling in Arabidopsis. Science 318:1302–1305

    Article  CAS  Google Scholar 

  • Lisch DR, Freeling M, Langham RJ, Choy MY (2001) Mutator transposase is widespread in the grasses. Plant Physiol 125:1293–1303

    Article  CAS  Google Scholar 

  • Malik HS, Henikoff S, Eickbush TH (2000) Poised for contagion: evolutionary origins of the infectious abilities of invertebrate retroviruses. Genome Res 10:1307–1318

    Article  CAS  Google Scholar 

  • 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 33:1553–1563

    Article  CAS  Google Scholar 

  • 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 281:27512–27525

    Article  CAS  Google Scholar 

  • 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 3:320–333

    Article  CAS  Google Scholar 

  • 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 403:785–789

    Article  CAS  Google Scholar 

  • 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 140:227–234

    Article  CAS  Google Scholar 

  • Nakamura TM, Cech TR (1998) Reversing time: origin of telomerase. Cell 92:587–590

    Article  CAS  Google Scholar 

  • 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 141:4763–4771

    Article  CAS  Google Scholar 

  • 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 22:312–323

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 73:232–237

    Article  CAS  Google Scholar 

  • 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 38:101–106

    Article  Google Scholar 

  • 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 18:211–219

    Article  CAS  Google Scholar 

  • 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 12:391–399

    Article  Google Scholar 

  • Renfree MB (2010) Marsupials: placental mammals with a difference. Placenta 31(Suppl):S21–S26

    Article  Google Scholar 

  • 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 368:20120151

    Article  Google Scholar 

  • 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 18:597–609

    Article  CAS  Google Scholar 

  • Schüller M, Jenne D and Voltz R (2005) The human PNMA family: novel neuronal proteins implicated in paraneoplastic neurological disease. J Neuroimmunol 169:172–176

    Article  Google Scholar 

  • 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 40:243–248

    Article  CAS  Google Scholar 

  • 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 29:4079–4088

    Article  CAS  Google Scholar 

  • 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 48:646–653

    Article  CAS  Google Scholar 

  • 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:e55

    Article  Google Scholar 

  • Vanin EF (1985) Processed pseudogenes: characteristics and evolution. Annu Rev Genet 19:253–272

    Article  CAS  Google Scholar 

  • 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 61:481–490

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fumitoshi Ishino .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Kaneko-Ishino, T., Ishino, F. (2019). Cooperation and Competition in Mammalian Evolution. In: Pontarotti, P. (eds) Evolution, Origin of Life, Concepts and Methods. Springer, Cham. https://doi.org/10.1007/978-3-030-30363-1_15

Download citation

Publish with us

Policies and ethics