There is a narrow inevitability about Partridge and Barton's response1 to True and Lindquist's evolutionary interpretation of their remarkable finding: that the presence of the yeast prion [PSI+] releases cryptic phenotypic variation which allows cells to thrive in fluctuating environments and which may facilitate the establishment of new traits2.
Partridge and Barton hover between dismissal and marginalization — the last resting place of many new discoveries of genome and developmental dynamics that do not fit easily with the simplistic notion of so-called 'modern' Darwinism that DNA mutation and recombination are the sole heritable changes of state of concern to selection.
What is at stake is whether heritable prion-induced variability in protein size is just a “side effect of disrupted gene expression” or an evolved system for the release of phenotypic variation. Have biological systems evolved evolvability?
The yeast prion case is but the latest example in a long list of ways by which organisms increase variation during the intricate processes of transforming genotypic information into phenotypes. There is no need to remind Nature 's molecular genetics readers of the total phenomenology of differential promoter utilization, DNA modification, differential DNA and RNA splicing, RNA editing, and post-translational modification. To these, we can now add Lindquist's earlier report of stress-induced release of variation via heat-shock protein chaperones3 and the [PSI+] story.
All such systems — such as the DNA-based systems of recombinational variation released by sex, the proof-reading systems involved with DNA replication, and genetic redundancy resulting from genomic turnover — have surely been influenced willy-nilly by selection to produce an exploitable balance between the eternal contrasting needs of stasis and change4.
The complex systems of proteins and RNA that are part of such multiple checks and balances are not just side effects of something else supposedly more fundamental and selectable — they are of the essence of responsive developmental processes. Either all of these systems facilitate evolution or they all don't. Given our current ignorance, we can't pick and choose.
Partridge, L. & Barton, N. H. Nature 407, 457–458 (2000).
True, H. L. & Lindquist, S. L. Nature 407, 477–483 (2000).
Rutherford, S. L. & Lindquist, S. L. Nature 396, 336–342 (1998).
Dover, G. A. Dear Mr Darwin: Letters on the Evolution of Life and Human Nature (Weidenfeld and Nicolson, London, 2000).
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The American Journal of Human Genetics (2002)