Skip to main content
Springer Nature Link
Log in

All about levels: transposable elements as selfish DNAs and drivers of evolution

  • Published:
Biology & Philosophy Aims and scope Submit manuscript

Abstract

The origin and prevalence of transposable elements (TEs) may best be understood as resulting from “selfish” evolutionary processes at the within-genome level, with relevant populations being all members of the same TE family or all potentially mobile DNAs in a species. But the maintenance of families of TEs as evolutionary drivers, if taken as a consequence of selection, might be better understood as a consequence of selection at the level of species or higher, with the relevant populations being species or ecosystems varying in their possession of TEs. In 2015, Brunet and Doolittle (Genome Biol Evol 7: 2445–2457) made the case for legitimizing (though not proving) claims for an evolutionary role for TEs by recasting such claims as being about species selection. Here I further develop this “how possibly” argument. I note that with a forgivingly broad construal of evolution by natural selection (ENS) we might come to appreciate many aspects of Life on earth as its products, and TEs as—possibly—contributors to the success of Life by selection at several levels of a biological hierarchy. Thinking broadly makes this proposition a testable (albeit extraordinarily difficult-to-test) Darwinian one.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Canada)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Beatty J (1984) Chance and natural selection. Phil Sci 51:183–211

    Article  Google Scholar 

  • Booth A, Doolittle WF (2015) Eukaryogenesis, how special really? Proc Natl Acad Sci USA 112:10278–10285

    Article  Google Scholar 

  • Borrello ME (2005) The rise, fall and resurrection of group selection. Endeavour 29:43–47

    Article  Google Scholar 

  • Bouchard F (2008) Causal processes, fitness, and the differential persistence of lineages. Phil Sci 75:560–570

    Article  Google Scholar 

  • Bouchard F (2014) Ecosystem evolution is about variation and persistence, not populations and reproduction. Biol Theory 9:382–391

    Article  Google Scholar 

  • Bousios A, Gaut BS (2016) Mechanistic and evolutionary questions about epigenetic conflicts between transposable elements and their plant hosts. Curr Op Plant Biol 30:123–133

    Article  Google Scholar 

  • Brandon R (1982) The levels of selection. PSA 1982(1):315–323

    Google Scholar 

  • Brenner S (1998) Refuge of spandrels. Curr Biol 8(19):R669

    Article  Google Scholar 

  • Britten RJ, Davidson EH (1969) Gene regulation for higher cells: a theory. Science 165:349–357

    Article  Google Scholar 

  • Brunet TDP, Doolittle WF (2015) Multilevel selection theory and the evolutionary functions of transposable elements. Genome Biol Evol 7:2445–2457

    Article  Google Scholar 

  • Brunet TDP, Doolittle WF, Bielawski JP (2021) The role of purifying selection in the origin and maintenance of complex function. Studies Hist Phil Biol Biomed Sci 87:125–135

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Comfort NC (1999) “The real point is control”: the reception of Barbara McClintock’s controlling elements. J Hist Biol 32:133–162

    Article  Google Scholar 

  • Dawkins R (1976) The selfish gene. Oxford University Press, Oxford

    Google Scholar 

  • Dawkins R (2006) The selfish gene: 40th Anniversary. Oxford, Oxford University Press

    Google Scholar 

  • De Koning APJ, Gu W, Castoe TA, Batzer MA, Pollock DD (2011) Repetitive elements may comprise over two-thirds of the human genome. PLoS Genet 7:e1002384

    Article  Google Scholar 

  • Doolittle WF (2017) Making the most of clade selection. Phil Sci 84:275–295

    Article  Google Scholar 

  • Doolittle WF (2018) We simply cannot go on being so vague about ‘function.’ Genome Biol 19:223

    Article  Google Scholar 

  • Doolittle WF (2019) Making evolutionary sense of Gaia. Trends Ecol Evol 34:889–894

    Article  Google Scholar 

  • Doolittle WF, Brunet TDP (2017) On causal roles and selected effects: our genome is still mostly junk. BMC Biol 15:116

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Dubin MJ, Scheid OM, Becker C (2018) Transposons: a blessing curse. Curr Op Plant Biol 42:23–29

    Article  Google Scholar 

  • Ecker JR, Bickmore WA, Barroso I, Pritchard JK, Gilad Y, Segal E (2012) ENCODE explained. Nature 489:52–54

    Article  Google Scholar 

  • Elliott TA, Gregory TR (2015) What’s in a genome? The C-value enigma and the evolution of eukaryotic genome content. Phil Trans Roy Soc B 370:20140331

    Article  Google Scholar 

  • Eşanu A (2018) A backward question about multilevel selection: Can species selection help disentangle the notion of group selection? In: Jeler C (ed) Multilevel selection and the theory of evolution. Palgrave Pivot, London

    Google Scholar 

  • Feschotte C (2008) Transposable elements and the evolution of regulatory networks. Nat Rev Genet 9:397–405

    Article  Google Scholar 

  • Fultz D, Choudury SG, Slotkin RK (2015) Silencing of active transposable elements in plants. Curr Op Plant Biol 27:67–76

    Article  Google Scholar 

  • Garson J (2021) Do Transposable Elements Have Functions of Their Very Own? Biol Philos (this issue)

  • Germain P-L, Ratti E (2021) A relic of design: against proper function in biology. Biol Philos (this issue)

  • Gildenhuys P (2019) Natural Selection, The Stanford Encyclopedia of Philosophy (Winter 2019 Edition), Edward N. Zalta (ed.). Accessed 20 April 21. URL = https://plato.stanford.edu/archives/win2019/entries/natural-selection/

  • Godfrey-Smith P (2012) Darwinism and cultural change. Philos Trans R Soc Lond B 367:2160–2170

    Article  Google Scholar 

  • Gould SJ (1983) Hen’s teeth and horse’s toes: further reflections in natural history. WW Norton, New York

    Google Scholar 

  • Gould SJ, Lewontin RC (1979) The spandrels of san marco and the panglossian paradigm: a critique of the adaptationist programme. Proc Roy Soc Lond B 205:581–598

    Article  Google Scholar 

  • Gould SJ, Vrba ES (1986) The hierarchical exapansion of sorting and selection: sorting and selection cannot be equated. Paleobiology 12:217–228

    Article  Google Scholar 

  • Gregory TR (2004) Macroevolution, hierarchy theory, and the C-value enigma. Paleobiology 30:179–202

    Article  Google Scholar 

  • Gregory TR, Elliott TA, Linquist S (2016) Why genomics needs multilevel evolutionary theory. In: Eldredge N, Pievani T, Serrelli E, Tёmkin I (eds) Evolutionary theory: a hierarchical perspective. University of Chicago Press, Chicago, pp 137–150

    Google Scholar 

  • Harold FM (2014) In search of history: the evolution of life’s building blocks. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Hickey D (1982) Selfish DNA: a sexually transmitted nuclear parasite. Genetics 101:519–531

    Article  Google Scholar 

  • Hill T, Betancourt AJ (2018) Extensive exchange of transposable elements in the Drosophila pseudoobscura group. Mob DNA. https://doi.org/10.1186/s13100-018-0123-6

    Article  Google Scholar 

  • Ho EKH, Agrawal AF (2017) Aging asexual lineages and the evolutionary maintenance of sex. Evolution 71:1865–1875

    Article  Google Scholar 

  • Hodge M.l.S. (1987) Natural selection as a causal, empirical, and probabilistic theory. In: LorenzKruger (ed) The probabilistic revolution. MIT Press, Cambridge, MA, pp 233–270

    Google Scholar 

  • Jablonski D (2007) A multilevel exploration. Science 316:1428–1430

    Article  Google Scholar 

  • Jablonski D (2008) Species selection: theory and data. Ann Rev Ecol Evol Syst 39:501–524

    Article  Google Scholar 

  • Jankovic S, Cirkovic MM (2016) Evolvability as an evolved ability: the coding concept as an arch-unit of natural selection. Orig Life Evol Biosphere 46:67–79

    Article  Google Scholar 

  • Johnson R, Guigó R (2014) The RIDL hypothesis: transposable elements as functional domains of long noncoding RNAs. RNA 20:959–976

    Article  Google Scholar 

  • Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Kleckner N (1981) Transposable elements in prokaryotes. Ann Rev Genet 15:341–404

    Article  Google Scholar 

  • Kremer SC, Linquist S, Saylor B, Elliott TA, Gregory TR, Cottenie K (2020) Transposable element persistence via potential genome-level ecosystem engineering. BMC Genom. https://doi.org/10.1186/s12864-020-6763-1

    Article  Google Scholar 

  • Lavialle C, Cornelis G, Dupressoir EC, Heidmann O, Vernochet C, Heidman T (2013) Paleovirology of ‘syncytins’, retroviral env genes exapted for a role in placentation. Phil Trans Roy Soc B 368:20120507

    Article  Google Scholar 

  • Lee H, Zhang Z, Krause HM (2019) Long noncoding RNAs and repetitive elements: junk or intimate evolutionary partners. Trends Genet 35:892–902

    Article  Google Scholar 

  • Linquist S, Saylor B, Cotterie K, Elliott TA, Kremer SC, Gregory TR (2013) Distinguishing ecological from evolutionary approaches to transposable elements. Biol Rev 88:573–584

    Article  Google Scholar 

  • Linquist S, Doolittle WF, Palazzo A (2020) Getting clear about the F-word in genomics. PLoS Genet 16:e1008702

    Article  Google Scholar 

  • Lynch M (2007) The frailty of adaptive hypotheses for the origin of organismal complexity. Proc Natl Acad Sci USA 104:8597–8604

    Article  Google Scholar 

  • Lynch M (2010) Evolution of the mutation rate. Trends Genet 26:345–352

    Article  Google Scholar 

  • McClintock B (1956) Controlling elements and the gene. Cold Spring Harbor Symp Quant Biol 21:197–216

    Article  Google Scholar 

  • Mills SK, Beatty JH (1979) The propensity interpretation of fitness. Phil Sci 46:263–286

    Article  Google Scholar 

  • Mills DR, Peterson RL, Spiegelman S (1967) An extracellular Darwinian experiment with a self-duplicaing nucleic acid molecule. Proc Natl Acad Sci USA 58:217–224

    Article  Google Scholar 

  • Millstein RL (2005) Selection vs. drift: a response to Brandon’s reply. Biol Philos 20:171–175

    Article  Google Scholar 

  • Millstein R (2010) The concepts of population and metapopulation in evolutionary biology and ecology. In: Bell M, Futuyma D, Eames Levinton J (eds) Evolution since darwin: the first 100 years. Sinauer, Sunderland

    Google Scholar 

  • Naito K, Zhang F, Tsukiyama T, Saito H, Hancock CN, Richardsim AO, Okumoto Y, Tanisaka T, Wessler SR (2009) Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 461:1130–1134

    Article  Google Scholar 

  • Nielson R (2009) Adaptationism—30 years after Gould and Lewontin. Evolution 63:2487–2490

    Article  Google Scholar 

  • Okasha S (2006) Multilevel selection and the major transitions in evolution. Phil Sci 72:1013–1025

    Article  Google Scholar 

  • Orgel LE, Crick FHC (1980) Selfish DNA: the ultimate parasite. Nature 284:604–607

    Article  Google Scholar 

  • Palazzo AF, Lee ES (2015) Non-coding RNA: what is functional and what is junk”. Front Genet. https://doi.org/10.3389/fgene.2015.00002

    Article  Google Scholar 

  • Pigliucci M (2008) Is evolvability evolvable? Nat Revs Genet 9:75–82

    Article  Google Scholar 

  • Platt RN II, Vandewege MW, Ray DA (2018) Mammalian transposable elements and their impacts on genome evolution. Chromosome Res 26:25–43

    Article  Google Scholar 

  • Rabosky DL, McCune AR (2010) Reinventing species selection with molecular phylogenies. Trends Ecol Evol 25:68–74

    Article  Google Scholar 

  • Resnick DB (1991) How-possibly explanations in biology. Acta Biotheor 39:141–149

    Article  Google Scholar 

  • Rieseberg LH (2001) Chromosomal rearrangements and speciation. Trends Ecol Evol 16:351–358

    Article  Google Scholar 

  • Rosenberg A, Bouchard F (2015) "Fitness", The Stanford Encyclopedia of Philosophy (Fall 2015 Edition), Edward N. Zalta (ed.). Accessed 09 Dec 21. URL = <https://plato.stanford.edu/archives/fall2015/entries/fitness/>.

  • Roughgarden J (2019) Holobiont evolution: model with vertical vs horizontal microbiome transition. bioRxiv. https://doi.org/10.1101/465310

    Article  Google Scholar 

  • Sandler L, Novitski E (1957) Meiotic drive as an evolutionary force. Am Nat 91:105–110

    Article  Google Scholar 

  • Sober E (1984) The nature of selection: evolutionary theory in philosophical focus. University of Chicago Press, Chicago

    Google Scholar 

  • Sober E (1992) Sceening-off and the units of selection. Phil Sci 59:142–152

    Article  Google Scholar 

  • Sober E, Wilson DS (2011) Adaptation and natural selection revisited. J Evol Biol 24:462–468

    Article  Google Scholar 

  • Van Valen LM (1989) Three paradigms of evolution. Evolut Theory 9:1–17

    Google Scholar 

  • Waples RS, Gaggliotti O (2006) What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol Ecol 15:1419–1439

    Article  Google Scholar 

  • Warren IA, Naville M, Chalopin D, Levin P, Burger CS, Galiana D, Volff J-N (2015) Evolutionary impact of transposable elements on geneomic diversity and lineage-specific innovation in vertebrates. Chromosome Res 23:505–531

    Article  Google Scholar 

  • Williams GC (1966) Adaptation and natural selection: a critique of some current evolutionary thought. Princeton, Princeton University Press

    Google Scholar 

  • Zeh DW, Zeh JA, Ishida Y (2009) Transposable elements and an epigenetic basis for punctuated equilibria. BioEssays 31:715–726

    Article  Google Scholar 

Download references

Funding

This study was funded by the Natural Sciences and Engineering Research Council of Canada (grant GLDSU447989), New Frontiers in Research Fund (grant NFRFE-2019–00703, and the Gordon and Betty Moore Foundation (GBMF9729, https://doi.org/10.37807/GBMF9729).

Author information

Authors and Affiliations

  1. Department of Biochemistry and Molecular Biology and Department of Philosophy, Dalhousie University, Halifax, NS, Canada

    W. Ford Doolittle

Authors
  1. W. Ford Doolittle
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to W. Ford Doolittle.

Ethics declarations

Conflict of interest

I have no competing financial or non-financial interests. I thank David Haig for making me realize that inserted TE copies are, as alleles, at best fixed by drift, and Stefan Linquist and Ryan Gregory for commenting on this manuscript.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Doolittle, W.F. All about levels: transposable elements as selfish DNAs and drivers of evolution. Biol Philos 37, 24 (2022). https://doi.org/10.1007/s10539-022-09852-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10539-022-09852-3

Keywords

Search

Navigation