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The ecology of the genome — mobile DNA elements and their hosts

Key Points

  • Because mobile DNA sequences replicate during transposition and can harm their hosts, they can be seen as selfish DNA sequences.

  • The interaction between mobile DNA sequences and their hosts makes the genome analogous to an ecological community, and many of the questions about the mobile DNA–host interaction have parallels with ecological questions.

  • Some of these questions are those that determine the expected abundance and diversity of mobile DNA sequences in the genome, and the factors that determine whether mobile DNA sequences will evolve to regulate their own activities.

  • Movement between host species creates a situation for transposable elements that is analogous to that of species living as metapopulations.

  • Beneficial effects for hosts from their interactions with mobile DNA sequences might include both short- and longer-term phenomena.

  • Benefits from the use of this ecological analogy might be in the identification of useful questions about transposable-element biology and evolution.

Abstract

The genomes of multicellular eukaryotes provide information that determines the phenotype. However, not all sequences in the genome are required for this purpose. Other sequences are often selfish in their actions and interact in complex ways. Here, an analogy is developed between the components of the genome, including mobile DNA elements, and an ecological community. Unlike ecological communities, however, the slow rates at which genomes change allow us to reconstruct patterns of interaction that stretch back tens or hundreds of millions of years.

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Figure 2: The life-cycle of a DNA transposon35,36.
Figure 1: The spread of an invading transposable element to an equilibrium created by a balance between the forces of transposition, deletion and selection.

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Acknowledgements

I thank L. Johnson, R. Edwards, H. Nicholas, M. Carr, P. Emery, R. Duddington, T. Robinson, J. McGraw and R. Badge for stimulating discussions about mobile DNAs. I also thank the Biotechnology and Biological Sciences Research Council for financial support.

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FURTHER INFORMATION

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Glossary

FITNESS

The expected ability of an organism to survive and reproduce, measured as the number of surviving offspring that are produced. Inclusive fitness is a broader term that includes benefits that are accrued to relatives of an individual.

ECOLOGICAL NICHE

The role of a species of organisms in an ecological community, defined by the resources that the species requires from its environment. The 'competitive exclusion principle' implies that species can only stably coexist if they have different ecological niches.

OPTIMAL FORAGING THEORY

A theory that is designed to predict the foraging behaviour that maximizes food intake per unit time.

SELFISH DNA

Sequences of DNA that accumulate in the genome through non-selective means, and which have a negative effect on the fitnesses of their hosts.

SINE SEQUENCE

A short interspersed element sequence — this is a retroposon sequence of less than 500 bp in length that does not encode the protein activities required for its movement.

LINE SEQUENCE

A long interspersed element sequence — typically used for non-long terminal repeat retrotransposons.

RETROTRANSPOSON

An autonomous transposable element that can move to a new location through an RNA intermediate. Long terminal repeat (LTR) retrotransposons have direct repeats of 300–500 bp of DNA at each end of the element. These sequences resemble the integrated proviruses of retroviruses. Non-LTR retrotransposons lack LTRs and the organization of their coding sequences is more diverged from that of retroviral sequences.

RETROPOSON

A mobile DNA sequence that can move to new locations through an RNA intermediate.

AUTONOMOUS ELEMENT

A transposable element that can supply all the requirements in both cis and trans for its own movement. In the case of a DNA transposon, this would include the trans-acting transposase protein and the element termini, required in cis for movement. A non-autonomous element would possess only the cis-acting sequences and would have to be supplied with transposase to move.

TELEOST

The group of bony fishes of the subclass Teleostei.

PANMICTIC

Referring to unstructured (random-mating) populations.

GENETIC DRIFT

Random changes in allele frequency that occur because the genes appearing in offspring are not a perfectly representative sample of the parental genes (for example, in small populations).

EFFECTIVE POPULATION SIZE

(Ne). The size of a population measured by the expected effect (through genetic drift) of the population size on genetic variablity. Ne is related to, but never exceeds, the actual population size (N).

DNA TRANSPOSON

A mobile DNA sequence that moves to new genomic locations through a DNA route, rather than through an RNA intermediate. This movement is catalysed by the action of a transposase protein that is encoded by an autonomous element.

METAPOPULATION

A collection of populations of a species found in differing geographic locations and with restricted gene flow (exchange of genes) between the populations.

RNA INTERFERENCE

The process by which dsRNA silences homologous genes.

SELECTIVE SWEEP

The process by which new favourable mutations become fixed so quickly that physically linked alleles also become fixed by 'hitch-hiking'.

TROPHIC

Of or involving the feeding habits or food relationship of different organisms in a food chain.

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Brookfield, J. The ecology of the genome — mobile DNA elements and their hosts. Nat Rev Genet 6, 128–136 (2005). https://doi.org/10.1038/nrg1524

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