Evolution of genome size: new approaches to an old problem

doi:10.1016/S0168-9525(00)02157-0

Trends in Genetics

Volume 17, Issue 1, 1 January 2001, Pages 23-28

https://doi.org/10.1016/S0168-9525(00)02157-0 Get rights and content

Abstract

Eukaryotic genomes come in a wide variety of sizes. Haploid DNA contents (C values) range >80 000-fold without an apparent correlation with either the complexity of the organism or the number of genes. This puzzling observation, the C-value paradox, has remained a mystery for almost half a century, despite much progress in the elucidation of the structure and function of genomes. Here I argue that new approaches focussing on the genetic mechanisms that generate genome-size differences could shed much light on the evolution of genome size.

Section snippets

‘Adaptive’ versus ‘junk DNA’ theories of genome-size evolution

Traditionally, theories of genome-size evolution primarily attempted to solve the puzzle of the apparent wastefulness of Nature; that is,why would many genomes have vast amounts of extra DNA considering the actual informational needs of the organism? There are two broad classes of explanations.

The ‘adaptive’ theories postulate an adaptive function for this extra DNA given that DNA abundance, rather than its information content, can have a direct and significant effect on phenotype ⁴ (Box 1).

Evolutionary forces affecting genome size

The current dichotomy between adaptive and junk DNA theories places the focus squarely on the question of whether extra DNA benefits the organism. But could there be more to it? I propose that by focussing exclusively on the question of the function (or lack of thereof) of extra DNA, the current debate obscures differences between various evolutionary explanations that might also be relevant. The easiest way to see this is to cast the question of genome-size evolution in terms of population

Distinguishing evolutionary forces of genome-size change

Given the multitude of genetic and population processes involved, the main challenge of the approach I am advocating is to find a way of distinguishing among them and to studying them individually.

One way to distinguish among the forces acting on genome size is to consider the timescale over which these forces could be effective, as different mutational mechanisms act on very different timescales. The activity of TEs is relatively fast, potentially amplifying the transposable-element copy

Global nature of forces affecting genome size

Another way to differentiate among multiple forces acting on genome size is to consider the scope of their action. Some forces, such as natural selection acting on a trait correlated with total genome size, are global in the sense that they affect the size of all genomic sequences, provided that these sequences are free to vary in size and that size variation exists. For example, if a lineage experiences an increased selection for a shorter developmental time (and therefore for more rapid DNA

Measuring individual forces

How can we assess the relative importance of particular mechanisms as forces of this genome-size change? As genome-size changes are reflected in all genomic components, we cannot answer this question simply by testing whether any one particular class of sequences is amplified in large genomes or reduced in compact ones. The action of any global force would produce very similar long-term effects.

What we need are direct experimental studies of the strength of the individual mechanisms of

Conclusion

The question of the C-value paradox has puzzled us for almost half a century. For much of this time the debate has centered on whether the vast amounts of noncoding DNA have any functional, adaptive role. This question needs to be settled if we are to understand fully the evolution of genome size. However, I believe the primary focus on this one question distracts us from other essential questions. How important is genetic drift in genome-size evolution? Do mutational rates of DNA addition and

Acknowledgements

I thank M. Siegal, D. Hartl, D. Bensasson, T. Gregory and E. Zuckerkandl for very helpful comments. Comments by the two anonymous referees and the editor helped to improve the manuscript significantly.

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Trends in Genetics

OpinionEvolution of genome size: new approaches to an old problem

Abstract

Section snippets

‘Adaptive’ versus ‘junk DNA’ theories of genome-size evolution

Evolutionary forces affecting genome size

Distinguishing evolutionary forces of genome-size change

Global nature of forces affecting genome size

Measuring individual forces

Conclusion

Acknowledgements

Mol. Biol. Evol.

Plant Mol. Biol.

Annu. Rev. Biochem.

Gene

The DNA content of animal cells and its evolutionary significance

J. Gen. Physiol.

The genetic organization of chromosomes

Annu. Rev. Genet.

The Eukaryotic Genome in Development and Evolution

The duration of meiosis

Proc. R. Soc. Lond. B Biol. Sci.

Nuclear volume control by nucleoskeletal DNA, selection for cell volume and cell growth rate, and the solution of the DNA C-value paradox

J. Cell Sci.

Buffering: a possible passive-homeostasis role for redundant DNA

J. Theor. Biol.

A possible function of constitutive heterochromatin: the bodyguard hypothesis

Genetics

Selfish DNA: the ultimate parasite

Nature

Selfish genes, the phenotype paradigm and genome evolution

Nature

Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid

Nature

The molecular basis of P-M hybrid dysgenesis: the role of the P element, a P-strain specific transposon family

Cell

Transposable elements in Drosophila melanogaster

Diverse transposable elements are mobilized in hybrid dysgenesis in Drosophila virilis

Proc. Natl. Acad. Sci. U.S.A.

Regulation of mutator activities in maize

Basic Life Sci.

From the cover: genome evolution of wild barley (Hordeum spontaneum) by BARE-1 retrotransposon dynamics in response to sharp microclimatic divergence

Proc. Natl. Acad. Sci. U.S.A.

A demonstrable local and geometric increase in the chromosomal DNA of Chironomous

Experientia.

Nuclear DNA variation in Allium

Heredity

Constraints upon the organization and evolution of chromosomes in Allium

Theor. Appl. Genet.

Evolution of genome size in Allium (Alliacea)

Plant Syst. Evol.

Plant DNA contents and systematics

Opinion
Evolution of genome size: new approaches to an old problem