parison of X with Y results in the figure consistent with expectations, but comparingX with autosomes suggests a much higherfigure10.

Although this latter discrepancy is notapparent from human data, analyses of primate and rodent sequences have revealeda further curiosity: not only does mutationrate vary along chromosomes11–13, but alsodifferent autosomes have remarkably differ-ent rates of evolution12,14. As all autosomesundergo the same number of replications,perhaps this will be the next clue to under-standing the causes of mutation. ■

Laurence D. Hurst is in the Department of Biologyand Biochemistry, University of Bath, Bath BA2 7AY, UK. e-mail: l.d.hurst@bath.ac.ukHans Ellegren is in the Department of EvolutionaryBiology, Evolutionary Biology Centre,

Uppsala University, 752-36 Uppsala, Sweden.e-mail: hans.ellegren@ebc.uu.se1. Crow, J. F. Nature Rev. Genet. 1, 40–47 (2000).

2. Hurst, L. D. & Ellegren, H. Trends Genet. 14, 446–452 (1998).

3. Chang, B. H. J., Shimmin, L. C., Shyue, S. K., Hewett-Emmett,

D. & Li, W.-H. Proc. Natl Acad. Sci. USA 91, 827–831 (1994).

4. Risch, N., Reich, E. W., Wishnick, M. M. & McCarthy, J. G.

Am. J. Hum. Genet. 41, 218–248 (1987).

5. Tiemann-Boege, I. et al. Proc. Natl Acad. Sci. USA 99,

14952–14957 (2002).

6. Wilkin, D. J. et al. Am. J. Hum. Genet. 63, 711–716 (1998).

7. Kluwe, L. et al. Neurogenetics 3, 17–24 (2000).

8. Miyata, T., Hayashida, H., Kuma, K., Mitsuyasu, K. & Yasunaga,

T. Cold Spring Harb. Symp. Quant. Biol. 52, 863–867 (1987).

9. Makova, K. D. & Li, W. H. Nature 416, 624–626 (2002).

10.Smith, N. G. C. & Hurst, L. D. Genetics 152, 661–673 (1999).

11.Matassi, G., Sharp, P. M. & Gautier, C. Curr. Biol. 9, 786–791

(1999).

12.Lercher, M. J., Williams, E. J. B. & Hurst, L. D. Mol. Biol. Evol.

18, 2032–2039 (2001).

13.Smith, N. G. C., Webster, M. T. & Ellegren, H. Genome Res. 12,

1350–1356 (2002).

14.Ebersberger, I., Metzler, D., Schwarz, C. & Paabo, S. Am. J.

Hum. Genet. 70, 1490–1497 (2002).

The hydrological cycle usually refers tothe process by which water cyclesthrough the atmosphere, rivers and

ocean, and round again. But is there anotherhydrological cycle, one that circulates waterthrough the depths of the Earth? It has longbeen suspected1 that surface material can be carried to the Earth’s deep interior by subduction of ocean crust and associatedmantle, and then returned to the surface by plumes rising through the mantle. In particular, from isotope data on basalt rockserupted on oceanic islands, it has seemedthat mantle plumes can carry deeply sub-ducted oceanic crust and sediment2, as wellas the residue of oceanic crust creation (theoceanic lithosphere)3, from depth back to the surface.

Does this process include relativelyvolatile species, such as water and carbondioxide? The results reported by Dixon et al.4

on page 385 of this issue suggest not, at leastto any great extent. They find that water iscycled much less efficiently in this way thanmight be expected — indeed, plumes thatapparently contain material recycled fromthe Earth’s surface contain less, not more,water than plumes dominated by the so-called ‘common component’, such as thatbeneath Iceland.

Magma readily gives up water at low pres-sure, the water escaping to the atmosphereduring, and even before, eruption. So deter-mining the water content of magma can bedifficult. At depths of 1,000 m or more in the

ocean, however, the pressure is sufficient formagma to retain its water as it quenches toglass by contact with sea water. Much of thework on volatiles in magmas has thereforecentred on quenched glass recovered fromsubmarine eruptions. These studies haveestablished that when the mantle melts,hydrogen behaves much like the rare-earthelement cerium5,6. To get around the varia-tions in water introduced by partial meltingand fractional crystallization, the H2O/Ceratio can be used to compare the relativeamounts of water in different magmas.Dixon et al.4 determined the water content ofsubmarine glasses erupted on regions of theMid-Atlantic Ridge thought to be influencedby mantle plumes. The water content ofmany of these basalts is surprisingly low, theH2O/Ce ratios being lower than in manyother submarine basalts at places such asEaster Island7.

Furthermore, samples from the Discov-ery plume in the South Atlantic and theGreat Meteor plume in the North Atlanticdisplay a negative correlation between theratios of H2O/Ce and of 87Sr/86Sr. The significance of this relationship is that itshows that the water deficiency is present inthe mantle that produced the basalts, and the strontium isotopes also provide insightinto the origin of that mantle. The 87Sr/86Srratio varies in the Earth only because of thevery slow decay of 87Rb (rubidium) to 87Sr.Because the continental crust is enriched inRb, the crust has a higher 87Sr/86Sr ratio than

does the mantle, so a high ratio in basalts cansignal the presence of recycled crustal mater-ial in the mantle. The most water-deficientsamples studied by Dixon et al. have thehighest 87Sr/86Sr ratios, suggesting that theyare derived from mantle containing recycledcrustal material.

In this respect, Dixon and colleagues’results are unexpected. One would havethought that recycled material would con-tain comparatively large amounts of water,for two reasons. First, marine sediments arerich in clay minerals, which can contain 10% or more water bound in their lattices.Second, circulating sea water hydrates thebasaltic oceanic crust, eventually raising itsstructurally bound water content to 2–5%by weight. Additional water is present in thepore space in both sediments and basalt.These water concentrations are far above theambient concentrations in the mantle, ofperhaps 0.03%. The amount of water carriedinto the mantle in subducted oceanic crustand sediment exceeds 121012 kg yr11 (ref.8), enough to drain the oceans in little morethan a billion years if the water were notreturned from the mantle.

Dixon et al. argue that the low water content of recycled material results fromefficient dehydration of the oceanic crustand sediment during subduction. This idea is not new. Release of water from sub-ducting oceanic crust has long been believedto cause the magma production fuelling volcanoes that ubiquitously sit atop subduc-tion zones9,10. Krakatoa, Mount St Helens,Mount Pinatubo and Soufriere Hills all lieabove subduction zones, and the notoriouslyexplosive nature of these and other such volcanoes is largely due to the high watercontent of their magmas. It is, however, a little surprising that the dehydration processis so efficient. Dixon et al. calculate that 92%of the water is extracted from subductingsediment, and 97% from the subductingoceanic crust. The deep hydrological cyclethus appears to be short-circuited, withmost subducted water quickly returning tothe surface through volcanism rather thanbeing carried into the deep mantle. In otherwords, the subducted material is effectivelyput through the wringer before it sinks veryfar into the mantle.

It would be interesting to compare theflux of water released by subduction-zonevolcanoes with estimates of the subductionflux and Dixon and colleagues’ calculateddehydration efficiency. It would also beinteresting to know if CO2 is released fromsubducting oceanic crust and sediment asefficiently as water is. These are difficulttasks, however — determining the watercontent of magmas erupted on land is prob-lematic, and CO2 is lost from magma evenmore readily than water.

Finally, the new results4 also point to theimportance of subduction-zone processes in

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366 NATURE | VOL 420 | 28 NOVEMBER 2002 | www.nature.com/nature

Earth science

Through the wringerWilliam M. White

Potentially huge amounts of water could be carried deep within the Earthby subducting oceanic crust. But it seems that most of that water isreleased, fuelling volcanism above subduction zones.

© 2002 Nature Publishing Group

shaping the composition of both the Earth’ssurface and its interior. Water released bydehydration could carry away much of thesoluble-element content of subducting crustand sediment. Any prediction of the compo-sition of deeply recycled crustal materialmust take account of these losses. ■

William M. White is in the Department of Earthand Atmospheric Sciences, Cornell University,Ithaca, New York 14853, USA.e-mail: white@geology.cornell.edu1. Armstrong, R. L. Rev. Geophys. 6, 175–199 (1968).

Evolution by natural selection requiresgenetic variation, and the ultimatesource of this variation is mutation —

random errors in genomic replication. Infact, because the fidelity of genomic repli-cation is influenced by genetic variation, the mutation rate is itself subject to naturalselection. Broad taxonomic data are consis-tent with this idea. Although mutation ratesper nucleotide vary by factors of up to a mil-lion among living things, the variation ingenomic mutation rates is less than a factorof a thousand. In RNA viruses, roughly onenucleotide per genome is incorrectly repro-duced in each replication; for retrovirusesthis genomic mutation rate is one per tenreplications; and it is one per 300 replicationsin DNA-based microbes, including DNAviruses and microorganisms1. Indeed, theremarkable similarity of genomic mutationrates within each of these groups may reflect deep underlying selective constraints,but its explanation remains a challenge toevolutionary biologists.

Writing in the journal Complexity, ChristelKamp and colleagues2 have now tackled the evolution of genomic mutation ratesfrom a fresh angle. By incorporating theimmune response as an explicit selectiveforce in standard ‘quasispecies’ models, theycalculate a viral genomic mutation rate that optimally balances the costs of too much andtoo little genetic variation.

Quasispecies theory3 was developed over30 years ago as a means of describing evolu-tion in populations of self-replicating RNAmolecules with high mutation rates (quasi-species is the term applied to closely relatedgenetic sequences that are affected as a groupby natural selection). But it was soon recog-nized that quasispecies theory made a usefultool for the study of viral evolution. Its mostfundamental prediction is the existence of

an error threshold. If the mutation rateexceeds this threshold, then all genomicinformation is irretrievably lost and the population becomes extinct in a kind ofmutational meltdown. In standard quasi-species theory, the simplifying assumption is made that evolutionary fitness is entirelygenetically determined and thus constantirrespective of the environment. Under thisassumption, a zero mutation rate is optimaland selection should always favour greaterfidelity of replication.

But viruses in their natural environmentstypically face rapidly changing selectionpressures as, for example, exerted by theimmune response of the body under viral

attack. So Kamp et al.2 have extended quasi-species theory to incorporate an adaptiveimmune response. In such an environment,a quasispecies becomes subject to a secondmutational threshold, this time a kind ofmutational ‘freeze’: if the mutation rate is too low, then the quasispecies does not keep pace with environmental change andbecomes extinct. An optimal genomic muta-tion rate must therefore lie somewherebetween mutational freeze and mutationalmeltdown (Fig. 1).

Kamp et al. have calculated this optimalgenomic mutation rate by finding the muta-tion rate that maximizes viral growth rate inthe presence of an immune response. Theyfind that the optimal mutation rate is givenby the ratio of the timespan required for thevirus to go through an entire replicationcycle to the timespan for the immune systemto mount a response to a new viral mutant.This result is reminiscent of population-genetic theories that have concluded that a rate of mutation that mirrors the rate of change of the selecting environment isoptimal for adaptive evolution4–6.

But Kamp et al. go one better than theseearlier models in that they incorporate theimmune response as an explicit selectiveforce. Comparing their quantitative pre-dictions with data for viral genomic mutation rates, they suggest that manyviruses, including HIV, replicate at the optimal genomic mutation rate. Interest-ingly, their result offers an explanation forthe intriguing constancy of genomic muta-tion rates within viral classes, because thevariation in the duration of viral life cyclesand the time to mount an immune responseis probably considerably smaller than thevariation in the rates of mutation pernucleotide.

The idea that viral mutation rates areoptimal for escaping host immune responsesis appealing7, but some questions remain.First, as previously mentioned, genomicmutation rates in RNA viruses are ten timeshigher than in retroviruses and 300 timeshigher than in DNA viruses. This doesn’t fitthe hypothesis of Kamp et al., because thereis no clear evidence for systematic differ-ences in the duration of viral life cycles or thedynamics of the immune responses to theseclasses of virus. Second, escape from theimmune system is not a universal feature ofviruses: many viruses may survive by trans-mission to new hosts before the immuneresponse takes effect.

In addition, the model of Kamp et al.forgoes some of the realism of population-genetic models for the evolution of mutationrates (reviewed in ref. 8). Such modelsexplicitly consider the fate of genes thatmodify replication and repair — changes inthe frequency of these modifier genes, due tothe rise or fall of linked beneficial or deleteri-ous mutations, affect the evolution of the

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NATURE | VOL 420 | 28 NOVEMBER 2002 | www.nature.com/nature 367

Virus evolution

The importance of being erroneousSebastian Bonhoeffer and Paul Sniegowski

Viruses must mutate to survive in the face of attack by their host’s immunesystem. A new model suggests that the viral mutation rate is optimized inan evolutionary trade-off between adaptability and genomic integrity.

Immune response

Deleterious mutations

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Figure 1 The evolution of viral genomicmutation rates. High mutation rates may enableviruses to escape the host’s immune responses,but low mutation rates reduce the probability ofdestroying essential viral genes. If the mutationrate is too high or too low, the viral populationbecomes extinct either because the geneticinformation is irretrievably lost or because thepopulation cannot keep pace with the immuneresponse. Kamp et al.2 have calculated a genomicmutation rate that optimally balances theseconstraints.

2. Hofmann, A. W. & White, W. M. Earth Planet. Sci. Lett. 57,

421–436 (1982).

3. Schaefer, B. F., Turner, S., Parkinson, I., Rogers, N. &

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4. Dixon, J. E., Leist, L., Langmuir, C. & Schilling, J.-G. Nature

420, 385–389 (2002).

5. Michael, P. Earth Planet. Sci. Lett. 131, 301–320 (1995).

6. Dixon, J. E. & Clague, D. A. J. Petrol. 42, 627–654 (2001).

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Berlin, 1981).

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