Partridge and Barton in their News and Views article1 on our paper2 make many interesting points, but they also misrepresent our hypothesis. Our main hypothesis is not that the yeast prion [PSI+] is maintained by natural selection because it aids evolution. This was the last of the three suggestions in our paper, and the one we least favoured. Partridge and Barton propose, as if it were an alternative view, that the increased variation [PSI+] produces is “a side effect of disrupted gene expression”. But this is obvious, and we never suggested otherwise.
The main point is that, no matter how it arose or is maintained, the prion has strong and remarkably varied effects on growth. This seems likely to permit survival in fluctuating environments and provides a plausible route to the evolution of new traits.
In our paper, we suggested that a capacity to accumulate silent variation and release it in a combinatorial fashion might facilitate evolutionary change. But this was not the motivation for our work, as suggested by Partridge and Barton. Rather, we asked if this very unusual form of inheritance might provide a selective advantage. It was the extraordinary diversity of the traits we observed that suggested broader implications. We never claimed these traits must be due to “large variations, involving several random changes”. Some might be, and this has important implications. But others might be due to something as simple as the addition of a few amino acids to a single kinase that increases its stability or prevents association with a repressor.
Finally, we did not suggest that “there is no path by which natural selection could construct [complex adaptations].” We are simply not convinced that stepwise, individually selected non-deleterious pathways are sufficient to explain all evolution.
When we discovered in earlier work that Hsp90 has a massive capacity to buffer morphogenetic variation and release that variation in response to environmental stress, we hypothesized that this protein might have a previously unappreciated impact on evolution, as a natural consequence of its special role in protein folding. We did not, however, as has been suggested3, claim that these properties evolved to this end.
It is disappointing that in many US schools the doctrine of creationism is given equal weight with the theory of evolution (see, for example, ref. 4). Plausible explanations for the sometimes puzzlingly rapid pace of evolution may help to counter arguments that evolution cannot have done what it is held to have done.
Partridge, L. & Barton, N. H. Nature 407, 457–458 (2000).
True, H. L. & Lindquist, S. L. Nature 407, 478–483 (2000).
Dickinson, W. J. & Seger, J. Nature 396, 336–342 (1998).
Lerner, S. L. Nature 407, 287–290 ( 2000).
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Nature Reviews Genetics (2005)
PLoS Biology (2004)
The American Journal of Human Genetics (2002)
Current Biology (2001)