Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

The role of selfish genetic elements in eukaryotic evolution

Key Points

  • Selfish genetic elements are very diverse and are a common feature of eukaryotes. Among them are: autonomously replicating elements, such as transposons; converting elements, such as homing endonucleases; segregation distorters, such as meiotic drive chromosomes; postsegregation distorters, such as the Medea locus of many insects and heritable microorganisms; and sex-ratio distorters.

  • Diversity of selfish genetic elements in a species is correlated with the outbreeding rate of that species — sexual reproduction enhances the spread of selfish elements and inbreeding decreases it.

  • The phenotype associated with selfish elements is often shown in hybrids that result from between-population crosses, because such crosses restore diversity and might alleviate the repression of selfish elements.

  • Selfish genetic elements can influence host speciation, for example Wolbachia-mediated cytoplasmic incompatibility promotes reproductive isolation among certain Drosophila species.

  • Segregation distorters, especially meiotic-drive sex chromosomes can lead to host extinction as a result of extreme sex-ratio bias.

  • Selfish genetic elements have a profound influence on the genetic architecture of eukaryotes, for example telomeres of Drosophila are made up of Het-A class I transposable elements, and the 'introns late' model proposes that introns have evolved from transposon-like elements. Methylation and RNA interference have been proposed to have evolved as host mechanisms designed to suppress transposition.

  • Sex-determination systems are very diverse in plants and animals. Sex determination might be inherently unstable as a result of a genetic conflict between Mendelian nuclear genes and non-Mendelian sex-ratio distorters, and this conflict might have a role in the evolution of sex-determination systems.

Abstract

'Selfish genetic elements', such as transposons, homing endonucleases, meiotic drive chromosomes and heritable microorganisms, are common features of eukaryotes. However, their importance in the evolution of eukaryotic genomes is still controversial. In this review, we discuss these diverse elements and their potential importance in the evolution of genetic systems, adaptation, and the extinction and birth of species.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Types of transposable element.
Figure 2: Homing endonucleases.
Figure 3: Model of Segregation distorter (Sd) action in Drosophila melanogaster.
Figure 4: Model of the evolution of sex-determination system in Armadillidium vulgare.

Similar content being viewed by others

References

  1. Werren, J. H., Nur, U. & Wu, C.-I. Selfish genetic elements. Trends Ecol. Evol. 3, 297–302 (1988).

    CAS  PubMed  Google Scholar 

  2. Hurst, L. D., Atlan, A. & Bengtsson, B. Genetic conflicts. Q. Rev. Biol. 71, 317–364 (1996).

    CAS  PubMed  Google Scholar 

  3. SanMiguel, P. et al. Nested retrotransposons in the intergenic regions of the maize genome. Science 274, 765–768 (1996).

    CAS  PubMed  Google Scholar 

  4. International Human Genome Sequencing Consortium. Initial sequencing and analysis of the human genome. Nature 409, 860–921 (2001).

  5. Biemont, C. & Cizeron, G. Distribution of transposable elements in Drosophila species. Genetica 105, 43–62 (1999).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Charlesworth, B., Sniegowski, P. & Stephan, W. The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371, 215–220 (1994).A review of the population genetics of transposable and other repetitive elements, detailing why transposons should be regarded as parasites.

    CAS  PubMed  Google Scholar 

  10. Kidwell, M. G. & Lisch, D. R. Transposable elements, parasitic DNA and genome evolution. Evolution 55, 1–24 (2001).A recent review of the importance of transposable elements in genome evolution that covers both mechanisms of suppression and evidence for co-option into host genome function.

    CAS  PubMed  Google Scholar 

  11. Bengtsson, B. O. Biased gene conversion as the primary function of recombination. Genet. Res. 47, 77–80 (1986).

    CAS  PubMed  Google Scholar 

  12. Dujon, B. Sequence of the intron and flanking exons of the mitochondrial 21S rRNA gene of yeast strains having different alleles at the omega and rib- 1 loci. Cell 20, 185–197 (1980).

    CAS  PubMed  Google Scholar 

  13. Gimble, F. S. & Thorner, J. Homing of a DNA endonuclease gene by meiotic conversion in Saccharomyces cerevisiae. Nature 357, 301–305 (1992).

    CAS  PubMed  Google Scholar 

  14. Lyttle, T. W. Segregation distorters. Annu. Rev. Genet. 25, 511–557 (1991).

    CAS  PubMed  Google Scholar 

  15. Hartl, D. L. Population dynamics of sperm and pollen killers. Theor. Appl. Genet. 42, 81–88 (1972).

    CAS  PubMed  Google Scholar 

  16. Jaenike, J. Sex-ratio meiotic drive in the Drosophila quinaria group. Am. Nat. 148, 237–254 (1996).

    Google Scholar 

  17. Jiggins, F. M., Hurst, G. D. D. & Majerus, M. E. N. How common are meiotically driving sex chromosomes? Am. Nat. 154, 481–483 (1999).

    CAS  PubMed  Google Scholar 

  18. Beukeboom, L. W. Bewildering Bs: an impression of the 1st B-chromosome conference. Heredity 73, 326–336 (1994).

    Google Scholar 

  19. Naito, T., Kusano, K. & Kobayashi, I. Selfish behaviour of restriction-modification systems. Science 267, 897–899 (1995).

    CAS  PubMed  Google Scholar 

  20. Cooper, T. F. & Heinemann, J. A. Postsegregational killing does not increase plasmid stability but acts to mediate exclusion of competing plasmids. Proc. Natl Acad. Sci. USA 97, 12643–12648 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Beeman, R. W., Friesen, K. S. & Denell, R. E. Maternal-effect selfish genes in flour beetles. Science 256, 89–92 (1992).An empirical paper detailing the discovery of Medea , a new type of selfish genetic element.

    CAS  PubMed  Google Scholar 

  22. Werren, J. H. Biology of Wolbachia. Annu. Rev. Entomol. 42, 587–609 (1997).

    CAS  PubMed  Google Scholar 

  23. Stouthamer, R., Breeuwer, J. A. J. & Hurst, G. D. D. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu. Rev. Microbiol. 53, 71–102 (1999).

    CAS  PubMed  Google Scholar 

  24. Hoffmann, A. A. & Turelli, M. in Influential Passengers: Inherited Microorganisms and Invertebrate Reproduction (eds O'Neill, S. L., Hoffmann, A. A. & Werren, J. H.) 42–80 (Oxford Univ. Press, Oxford, 1997).

    Google Scholar 

  25. Cosmides, L. & Tooby, J. Cytoplasmic inheritance and intragenomic conflict. J. Theor. Biol. 89, 83–129 (1981).This is a seminal paper discussing the nature of conflicts between genes inherited through the cytoplasm and the nucleus.

    CAS  PubMed  Google Scholar 

  26. Hurst, L. D. The incidences, mechanisms and evolution of cytoplasmic sex ratio distorters in animals. Biol. Rev. 68, 121–193 (1993).

    Google Scholar 

  27. Werren, J. H. The paternal sex ratio chromosome of Nasonia. Am. Nat. 137, 392–402 (1991).

    Google Scholar 

  28. Bestor, T. H. Sex brings transposons and genomes into conflict. Genetica 107, 289–295 (1999).

    CAS  PubMed  Google Scholar 

  29. Arkhipova, I. & Meselson, M. Transposable elements in sexual and ancient asexual taxa. Proc. Natl Acad. Sci. USA 97, 14473–14477 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Burt, A. & Trivers, R. Selfish DNA and breeding systems in flowering plants. Proc. R. Soc. Lond. B 265, 141–146 (1998).

    Google Scholar 

  31. Biemont, C., Aouar, A. & Arnault, C. Genome reshuffling of the copia element in an inbred line of Drosophila melanogaster. Nature 329, 742–744 (1987).

    CAS  PubMed  Google Scholar 

  32. Petrov, D. A., Schutzman, J. L., Hartl, D. L. & Lozovskaya, E. R. Diverse transposable elements are mobilized in hybrid dysgenesis in Drosophila virilis. Proc. Natl Acad. Sci. USA 92, 8050–8054 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Merçot, H., Atlan, A., Jacques, M. & Montchamp-Moreau, C. Sex-ratio distortion in Drosophila simulans: co-occurence of a meiotic driver and a supressor of drive. J. Evol. Biol. 8, 283–300 (1995).

    Google Scholar 

  34. Frank, S. A. The evolutionary dynamics of cytoplasmic male sterility. Am. Nat. 133, 345–376 (1989).

    Google Scholar 

  35. Laven, H. Crossing experiments with Culex strains. Evolution 5, 370–375 (1951).

    Google Scholar 

  36. Black, D. M., Jackson, M. S., Kidwell, M. G. & Dover, G. KP elements repress P-induced hybrid dysgenesis in Drosophila melanogaster. EMBO J. 6, 4125–4135 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Prud'homme, N., Gans, M., Masson, M., Terzian, C. & Bucheton, A. Flamenco, a gene controlling the gypsy retrovirus of Drosophila melanogaster. Genetics 139, 697–711 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Ginzburg, L. R., Bingham, P. M. & Yoo, S. On the theory of speciation induced by transposable elements. Genetics 107, 331–341.

  39. Frank, S. A. Divergence of meiotic drive-suppression systems as an explanation for sex biased hybrid sterility and inviability. Evolution 45, 262–267 (1991).

    PubMed  Google Scholar 

  40. Hurst, L. D. & Pomiankowski, A. N. Causes of sex ratio bias may account for unisexual sterility in hybrids: a new explanation for Haldane's rule and related phenomena. Genetics 128, 841–858 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Coyne, J. A. Genetics and speciation. Nature 355, 511–515 (1992).

    CAS  PubMed  Google Scholar 

  42. Hurst, G. D. D. & Schilthuizen, M. Selfish genetic elements and speciation. Heredity 80, 2–8 (1998).

    Google Scholar 

  43. Regner, L. P., Pereira, M. S. O., Alonso, C. E. V., Abdelhay, E. & Valente, V. L. S. Genomic distribution of P-elements in Drosophila willistoni and a search for their relationship with chromosomal inversions. J. Hered. 87, 191–198 (1996).

    CAS  PubMed  Google Scholar 

  44. Shoemaker, D. D., Katju, V. & Jaenike, J. Wolbachia and the evolution of reproductive isolation between Drosophilla recens and Drosophila subquinaria. Evolution 53, 1157–1164 (1999).

    PubMed  Google Scholar 

  45. Breeuwer, J. A. J. & Werren, J. H. Microorganisms associated with chromosome destruction and reproductive isolation between two insect species. Nature 346, 558–560 (1990).

    CAS  PubMed  Google Scholar 

  46. Bordenstein, S. R., O'Hara, F. P. & Werren, J. H. Wolbachia-induced bidirectional incompatibility precedes other hybrid incompatibilities in Nasonia. Nature 409, 707–710 (2001).A recent paper giving evidence that Wolbachia strains associated with creating reproductive isolation might be present before significant divergence for nuclear genes.

    CAS  PubMed  Google Scholar 

  47. Telschow, A., Hammerstein, P. & Werren, J. H. The effect of Wolbachia on genetic divergence between populations: mainland island model. Am. Zool. (in the press).

  48. Hamilton, W. D. Extraordinary sex ratios. Science 156, 477–488 (1967).

    CAS  PubMed  Google Scholar 

  49. Carvalho, A. B. & Vaz, S. C. Are Drosophila SR drive chromosomes always balanced. Heredity 83, 221–228 (1999).

    PubMed  Google Scholar 

  50. Lyttle, T. W. Experimental population genetics of meiotic drive systems. I. Pseudo-Y chromosomal drive as a means of eliminating cage populations of Drosophila melanogaster. Genetics 86, 413–445 (1977).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Jiggins, F. M., Hurst, G. D. D., Dolman, C. E. & Majerus, M. E. M. High prevalence of male-killing Wolbachia in the butterfly Acraea encedana. J. Evol. Biol. 13, 495–501 (2000).

    Google Scholar 

  52. Jiggins, F. M., Hurst, G. D. D. & Majerus, M. E. N. Sex-ratio-distorting Wolbachia causes sex-role reversal in its butterfly host. Proc. R. Soc. Lond. B 267, 69–73 (2000).

    CAS  Google Scholar 

  53. Stouthamer, R., Hurst, G. D. D. & Breeuwer, J. A. J. in Sex Ratio Distorters and Their Detection (ed. Hardy, I. C. W.) (Cambridge Univ. Press, Cambridge, UK, 2001).

    Google Scholar 

  54. Hoekstra, R. F. in The Evolution of Sex and Its Consequences (ed. Stearns, S. C.) 59–91 (Birkhauser, Basel, 1987).

    Google Scholar 

  55. Hickey, D. H. & Rose, M. R. in The Evolution of Sex: an Examination of Current Ideas (eds Michod, R. E. & Levin, B. R.) 161–175 (Sinauer Associates, Sunderland, Massachusetts, 1988).

    Google Scholar 

  56. Haig, D. & Grafen, A. Genetic scrambling as a defence against meiotic drive. J. Theor. Biol. 153, 531–558 (1991).

    CAS  PubMed  Google Scholar 

  57. Logsdon, J. M. Jr The recent origins of spliceosomal introns revisited. Curr. Opin. Genet. Dev. 8, 637–648 (1998).

    CAS  PubMed  Google Scholar 

  58. Selker, E. U. Gene silencing: repeats that count. Cell 97, 157–160 (1999).

    CAS  PubMed  Google Scholar 

  59. Jensen, S., Gassama, M. & Heidmann, T. Taming of transposable elements by homology-dependent gene silencing. Nature Genet. 21, 209–212 (1999).

    CAS  PubMed  Google Scholar 

  60. Ketting, R. F., Haverkamp, H. G., Van Luenen, A. M. & Plasterk, H. A. mut-7 of C. elegans, required for transposon silencing and RNA interference, is a homolog of Werner syndrome helicase and RNaseD. Cell 99, 133–141 (1999).

    CAS  PubMed  Google Scholar 

  61. Hammond, S. M., Caudy, A. A. & Hannon, G. J. Post-transcriptional gene silencing by double-stranded RNA. Nature Rev. Genet. 2, 110–119 (2001).

    CAS  PubMed  Google Scholar 

  62. Bird, A. P. Gene number, noise reduction and biological complexity. Trends Genet. 11, 94–100 (1995).

    CAS  PubMed  Google Scholar 

  63. Bestor, T. H. & Tycko, B. Creation of genomic DNA methylation patterns. Nature Genet. 12, 363–367 (1996).

    CAS  PubMed  Google Scholar 

  64. Yoder, J. A., Walsh, C. P. & Bestor, T. H. Cytosine methylation and the ecology of intragenomic parasites. Trends Genet. 13, 335–340 (1997).

    CAS  PubMed  Google Scholar 

  65. O'Neill, R. J. W., O'Neill, M. J. & Graves, J. A. M. Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid. Nature 393, 68–72 (1998).This paper details the effects of breakdown of transposable element suppression on the wallaby genome after loss of methylation in hybrids.

    CAS  PubMed  Google Scholar 

  66. Van Valen, L. A new evolutionary law. Evol. Theory 1, 1–30 (1973).

    Google Scholar 

  67. Bull, J. J. Evolution of Sex Determination Mechanisms (Benjamin Cummings, Inc., Menlo Park, California, 1983).

    Google Scholar 

  68. Werren, J. H. & Beukeboom, L. W. Sex determination, sex ratios and genetic conflict. Annu. Rev. Ecol. Syst. 29, 233–261 (1998).This review discusses the current evidence for a role of selfish genetic elements in the evolution of sex determination, and assesses their potential importance in this field.

    Google Scholar 

  69. Rousset, F., Bouchon, D., Pintureau, B., Juchault, P. & Solignac, M. Wolbachia endosymbionts responsible for various alterations of sexuality in arthropods. Proc. R. Soc. Lond. B 250, 91–98 (1992).

    CAS  Google Scholar 

  70. Rigaud, T. & Juchault, P. Conflict between feminizing sex ratio distorters and an autosomal masculizing gene in the terrestrial isopod Armadillidium vulgare Latr. Genetics 133, 247–252 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Caubet, Y., Hatcher, M. J., Mocquard, J.-P. & Rigaud, T. Genetic conflict and changes in heterogametic mechanisms of sex determination. J. Evol. Biol. 13, 766–777 (2000).

    Google Scholar 

  72. Saumitou-Laprade, P., Cuguen, J. & Vernet, P. Cytoplasmic male sterility in plants: molecular evidence and the nucleocytoplasmic conflict. Trends Ecol. Evol. 9, 431–435 (1994).

    CAS  PubMed  Google Scholar 

  73. Levskaya, O., Slot, F., Pavlova, M. & Pardue, M. L. Structure of the Drosophila HET-A transposon — a retrotransposon-like element forming telomeres. Chromosoma 103, 215–224 (1994).

    Google Scholar 

  74. Eickbush, T. H. Telomerase and retrotransposons: which came first? Science 277, 911–912 (1997)

    CAS  PubMed  Google Scholar 

  75. Nakamura, T. M. et al. Telomerase catalytic subunit homologs from fission yeast and humans. Science 277, 955–959 (1997).

    CAS  PubMed  Google Scholar 

  76. Van Gent, D. C., Mizuuchi, K. & Gellert, M. Similarities betweein initiation of V(D)J recombination and retroviral intregration. Science 271, 1592–1594 (1996).

    CAS  PubMed  Google Scholar 

  77. Agrawal, A., Eastman, Q. M. & Schatz, D. G. Transposition mediated RAG1 and RAG2 and its implications for the evolution of the immune system. Nature 394, 744–751 (1998).This study details evidence supporting the theory that parts of the V(D)J recombination system in developing lymphocytes were once components of a transposable element.

    CAS  PubMed  Google Scholar 

  78. Ganetsky, B. On the components of segregation distortion in Drosophila melanogaster. Genetics 86, 321–355 (1977).

    Google Scholar 

  79. Wu, C.-I., Lyttle, T. W., Wu, M.-L. & Lin, G.-F. Association between a satellite DNA-sequence and the responder of Segregation distorter in Drosophila melanogaster. Cell 54, 179–189 (1988).

    CAS  PubMed  Google Scholar 

  80. Merrill, C., Bayraktaroglu, L., Kusano, A. & Ganetzky, B. Truncated RanGAP encoded by the Segregation distorter locus of Drosophila. Science 283, 1742–1745 (1999).

    CAS  PubMed  Google Scholar 

  81. Keller, L. & Ross, K. G. Selfish genes: a green beard in the red fire ant. Nature 394, 573–575 (1998).This paper details the discovery of a selfish genetic element in ants that acts through the behaviour of the individual that carries it.

    CAS  Google Scholar 

  82. Stouthamer, R. in Influential Passengers: Inherited Microorganisms and Invertebrate Reproduction (eds O'Neill, S. L., Hoffmann, A. A. & Werren, J. H.) 102–124 (Oxford Univ. Press, Oxford, UK, 1997).

    Google Scholar 

  83. Rigaud, T. in Influential Passengers: Inherited Microorganisms and Invertebrate Reproduction (eds O'Neill, S. L., Hoffmann, A. A. & Werren, J. H.) 81–102 (Oxford Univ. Press, Oxford, UK, 1997).

    Google Scholar 

  84. Hurst, G. D. D., Hurst, L. D. & Majerus, M. E. N. in Influential Passengers: Inherited Microorganisms and Invertebrate Reproduction (eds O'Neill, S. L., Hoffmann, A. A. & Werren, J. H.) 125–154 (Oxford Univ. Press, Oxford, UK, 1997).

    Google Scholar 

Download references

Acknowledgements

J.H.W. thanks T. Eickbush for many interesting discussions on transposon evolution and S. Bordenstein for helpful discussions about heriTable microbes and meiotic drive; G.D.D.H. thanks M. Goddard for discussions of homing endonuclease dynamics. We thank L. Sacchi, and C. Bandi for providing figures. G.D.D.H. is supported by a BBSRC David Phillips Fellowship. Research support for J.H.W. was provided by the US National Science Foundation.

Author information

Authors and Affiliations

Authors

Related links

Related links

DATABASE LINKS

Sd

t-complex

Medea

flamenco

RAG1

RAG2

Glossary

FITNESS

A measure of the capacity to survive and reproduce.

SYMBIONT

An organism that lives in intimate contact (symbiosis) with another organism during most of its life.

SEGREGATION DISTORTION

Any distortion of meiosis or gametogenesis such that one of a pair of chromosomes in a heterozygote is recovered in greater than half of the progeny.

SUPERNUMERARY (B) CHROMOSOME

A chromosome that is non-essential to organismal function and might be present in zero, one, two or more copies per individual.

HOMING ENDONUCLEASE

An enzyme that cuts DNA at a sequence motif and inserts a copy of its own gene into the cut site.

GENE CONVERSION

A non-reciprocal recombination process that results in an alteration of the sequence of a gene to that of its homologue during meiosis.

FIXATION

Increase in allele frequency to the point where all individuals in a population are homozygous.

MEIOTIC DRIVE

Distortion of meiosis such that one of a pair of chromosomes in a heterozygote is recovered in greater than half of the progeny. A subset of segregation distortion.

CYTOPLASMIC INCOMPATIBILITY

A sperm–egg incompatibility usually associated with Wolbachia infections. Wolbachia modify the host sperm in testes and the same strain of Wolbachia must be present in the egg to rescue this modification. Absence of rescue results in incompatibility and zygotic lethality.

PANMICTIC POPULATION

A population in which the probability that any given male and female mate is equal for all individuals.

CYTOPLASMIC MALE STERILITY

Phenotype of male sterility in which the trait is carried on a cytoplasmically inherited gene. Occurs commonly in plants and is associated with mitochondrial mutations.

PARTHENOGENESIS

A form of reproduction in which eggs develop without being fertilized.

PARASITOID

An organism in which the adult is free living and lays eggs that hatch and develop in the body of another organism.

HYMENOPTERA

A large order of insects with four transparent wings that includes the bees, wasps, ants and sawflies.

REPRODUCTIVE ISOLATION

The condition in which barriers prevent or strongly limit reproduction between populations. Reproductive isolation can occur in many ways, but always has the same effect: no or few genes are exchanged between populations.

HYBRID DYSGENESIS

Breakdown of organismal function after crosses involving individuals from different populations. An example is P-element-mediated dysgenesis, in which crosses between males from populations bearing P elements and females from populations in which they are absent is associated with gonadal dysfunction and elevated deleterious mutation rates.

GENE FLOW

Movement of genes from one population to another.

HYBRID BREAKDOWN

A post-zygotic isolating mechanism in which the first-generation hybrids are viable and fertile, but subsequent generations of hybrids are inviable or infertile.

INTRONS LATE MODEL

A model that proposes that introns evolved from transposon-like group II elements and that the spliceosome machinery evolved to mitigate their negative effects.

V(D)J RECOMBINATION

A specialized form of recombination that assembles the genes that encode lymphocyte antigen receptors from variable (V), diversity (D) and joining (J) gene segments.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hurst, G., Werren, J. The role of selfish genetic elements in eukaryotic evolution. Nat Rev Genet 2, 597–606 (2001). https://doi.org/10.1038/35084545

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/35084545

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing