Key Points
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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.
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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.
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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.
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Selfish genetic elements can influence host speciation, for example Wolbachia-mediated cytoplasmic incompatibility promotes reproductive isolation among certain Drosophila species.
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Segregation distorters, especially meiotic-drive sex chromosomes can lead to host extinction as a result of extreme sex-ratio bias.
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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.
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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.
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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.
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Glossary
- FITNESS
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A measure of the capacity to survive and reproduce.
- SYMBIONT
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An organism that lives in intimate contact (symbiosis) with another organism during most of its life.
- SEGREGATION DISTORTION
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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
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A chromosome that is non-essential to organismal function and might be present in zero, one, two or more copies per individual.
- HOMING ENDONUCLEASE
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An enzyme that cuts DNA at a sequence motif and inserts a copy of its own gene into the cut site.
- GENE CONVERSION
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A non-reciprocal recombination process that results in an alteration of the sequence of a gene to that of its homologue during meiosis.
- FIXATION
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Increase in allele frequency to the point where all individuals in a population are homozygous.
- MEIOTIC DRIVE
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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
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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
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A population in which the probability that any given male and female mate is equal for all individuals.
- CYTOPLASMIC MALE STERILITY
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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
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A form of reproduction in which eggs develop without being fertilized.
- PARASITOID
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An organism in which the adult is free living and lays eggs that hatch and develop in the body of another organism.
- HYMENOPTERA
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A large order of insects with four transparent wings that includes the bees, wasps, ants and sawflies.
- REPRODUCTIVE ISOLATION
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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
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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
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Movement of genes from one population to another.
- HYBRID BREAKDOWN
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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
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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
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A specialized form of recombination that assembles the genes that encode lymphocyte antigen receptors from variable (V), diversity (D) and joining (J) gene segments.
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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
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DOI: https://doi.org/10.1038/35084545
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