so in the wild. The cognitivedemands for inventing suchtraditions thus appear to be easilymet, not only by chimpanzees butalso by other great apes. Ifinventions occur easily, a high rateof invention could in principlecontribute to making thedistribution of traditions disjunct.

In practice, however, there isa problem with this explanation.Chimpanzees are an old species:they closely resemble bonobos,a morphologically derived sisterspecies that split off at least1 million years ago [12]. Ifchimpanzees have been inventingand passing on traditions even foras short a period as 1 million years,the distribution of traditions wouldbe limited by the rate of inventiononly if the rate of invention werevanishingly low — much less than 1in every 10,000 years for example.The fact that chimpanzees haveinvented traditions while beingobserved by humans suggests thatevery population should have hadample opportunity to acquire it. Sothe rate of repeat inventionappears too high to account for thedistribution of a series ofidiosyncratic sets of chimpanzeetraditions.

If invention alone cannot explainwhy the unpredictable location oftraditions, we are forced to thinkabout a little-studied topic:extinction. The obviousexplanation for why Kibalechimpanzees do not dip for ants,Gombe chimpanzees do nothand-clasp-groom, or Bossouchimpanzees do not useleaf-napkins is that, although theirancestors did, the tradition diedout. Why extinctions shouldhappen regularly is unclear.Long-term studies will be neededto test how population bottlenecks,alternative fashions, individualpersonalities or other factors mightpromote rates of traditionextinction. Understanding theextinction of chimpanzee traditionsholds promise for explaining whyape culture has never blossomedas it did, critically, for humans.

Unfortunately the opportunitiesfor studying apes are disappearingrapidly due to extinction not just oftraditions, but of wholepopulations. But on the positiveside, Ebo nut-smashing is only one

of many recent tool-usingdiscoveries that in the 21st centuryinclude chimpanzee tool-kits in theCongo and the first gorilla tools inthe wild, as well as capuchinmonkey stone-tool-use in Brazil[13–15]. There is still an opportunityto learn much about the distributionof cultural variants, let alone whythey are vulnerable to extinction.

Happily, as Morgan and Abwe[7] hint, the process of studyingpopulations like Ebo often leads tothe establishment of a long-termresearch program, one of the mosteffective ways to promoteconservation. Their discovery thuspromises to benefit both scienceand conservation. If the newtradition proves idiosyncratic Ebowill become a site of particularinterest but whatever is foundthere, the big picture is clear: thecultural primatology of centralAfrica is still in its infancy.

References1. Savage, T.S., and Wyman, J. (1844).

Observations on the external charactersand habits of the Troglodytes Niger,Geoff.; and on its organization. BostonJ. Nat. Hist. 4, 362–386.

2. Yamakoshi, G. (2001). Ecology of tool usein wild chimpanzees: towardreconstruction of early hominid evolution.In Primate Origins of Human Cognitionand Behavior, T. Matsuzawa, ed. (Tokyo:Springer-Verlag), pp. 537–556.

3. McGrew, W.C. (1997). Why don’tchimpanzees in Gabon crack nuts? Int.J. Primatol. 18, 353–374.

4. Boesch, C., Marchesi, P., Marchesi, N.,Fruth, B., and Joulian, F. (1994). Is nutcracking in wild chimpanzees a culturalbehaviour? J. Hum. Evol. 26, 325–338.

5. Lonsdorf, E.V. (2006). What is the role ofmothers in the acquisition oftermite-fishing behaviors in wild

chimpanzees (Pan troglodytesschweinfurthii)? Anim. Cogn. 9, 36–46.

6. Biro, D., Inoue-Nakamura, N.,Tonooka, R., Yamakoshi, G., Sousa, C.,and Matsuzawa, T. (2003). Culturalinnovation and transmission of tool usein wild chimpanzees: evidence from fieldexperiments. Anim. Cogn. 6, 213–223.

7. Morgan, B.J., and Abwe, E.E. (2006).Chimpanzees use stone hammersin Cameroon. Curr. Biol. 16,R632–R633.

8. Mercader, J., Panger, M., and Boesch, C.(2002). Excavation of a chimpanzee stonetool site in the African rainforest. Science296, 1452–1455.

9. Whiten, A., Goodall, J., McGrew, W.C.,Nishida, T., Reynolds, V., Sugiyama, Y.,Tutin, C.E.G., Wrangham, R.W., andBoesch, C. (2001). Charting culturalvariation in chimpanzees. Behaviour 138,1481–1516.

10. de Waal, F.B.M., and Seres, M. (1997).Propagation of handclasp groomingamong captive chimpanzees. Am. J.Primatol. 43, 339–346.

11. Hayashi, M., Mizuno, Y., andMatsuzawa, T. (2005). How doesstone-tool use emerge? Introduction ofstones and nuts to naive chimpanzees incaptivity. Primates 46, 91–102.

12. Wrangham, R.W., and Pilbeam, D. (2001).African apes as time machines. In All apesgreat and small: chimpanzees, bonobos,and gorillas, Vol. 1, B.M.F. Galdikas,N. Briggs, L.K. Sheeran, G.L. Shapiro, andJ. Goodall, eds. (New York: KluwerAcademic/Plenum), pp. 5–18.

13. Breuer, T., Ndoundou-Hockemba, M., andFishlock, V. (2005). First observation of tooluse in wild gorillas. PLoS Biol. 3, 2041–2043.

14. Sanz, C., Morgan, D., and Gulick, S.(2004). New insights into chimpanzees,tools, and termites from the Congo Basin.Am. Nat. 164, 567–581.

15. Visalberghi, E., Fragaszy, D.M., Izar, P.,and Ottoni, E. (2005). Terrestriality andtool use. Science 308, 951.

Department of Anthropology, HarvardUniversity, Peabody Museum,11 Divinity Avenue, Cambridge,Massachusetts 02138, USA.E-mail: wrangham@fas.harvard.edu

DOI: 10.1016/j.cub.2006.07.031

DispatchR635

Molecular Biology: SilencingUnlimited

Heterochromatin domains are essential for normal chromosomefunctions. The Eri1 ribonuclease is a negative regulator of the RNAinterference machinery; recent studies have shown that, in fission yeastlacking Eri1, heterochromatin formation is more promiscuous.

Ricardo Almeida,Alessia Buscainoand Robin C. Allshire

Heterochromatin is the portion ofnuclear chromatin that maintainsa condensed state during the cellcycle and that provides specific

functions at various chromosomallocations, such as centromeresand telomeres. In the fission yeast,Schizosaccharomyces pombe,heterochromatin is formed atdistinct chromosomal regions:centromeres, the mating typelocus, telomeres and ribosomal

Current Biology Vol 16 No 16R636

HDACClr4HDAC Clr4

RITS RITS

Heterochromatin Euchromatin

Spreading

Epe1

tRNAB-boxes

Heterochromatin

Euchromatin

Euchromatin

Eri1

Epe1

Heterochromatin

Euchromatin

tRNAB-boxes

Spreading

C Eri1 modulates the strength of theRNAi signal delivered to chromatin

D Heterochromatin formation is morepromiscuous in the absence of Eri1

A Heterochromatin spreading is counteracted by boundaryelements and Epe1 activity

B Without Epe1 and boundary activity, heterochromatin can spreadpast its limits and silence nearby genes

active gene

Eri1

Bou

ndar

y

Acetylatednucleosomes

H3K9 methylatednucleosomes

Current Biology

Figure 1. Heterochromatin formation and spreading are tightly controlled in fissionyeast.

(A) Heterochromatin spreading (red arrow) is antagonized by two different knownprocesses: boundaries (grey box) containing either tRNA or B-box motifs; the ‘anti-silencer’ factor Epe1 (blue arrow). (B) In the absence of these two processes, hetero-chromatin is allowed to expand past its normal limits and repress genes in euchromatin(in orange). (C) RNA interference is involved in determining the sites of heterochromatinformation (nucleation). The RITS complex (in green) containing siRNAs (in red) recog-nizes a target locus and induces deacetylation and H3K9 methylation by HDAC andClr4 (hexagons). Eri1 antagonizes RNAi activity and limits its ability to nucleate. (D) Inthe absence of Eri1, the RNAi pathway is more active and can induce heterochromatinformation in chromosomal loci which are not typically engulfed in this structure (onthe right).

(r)DNA arrays. A commonfeature is that these regions areall composed of repetitivesequences which may facilitatetheir assembly intotranscriptionally silent chromatin.Several histone modificationsand histone binding proteins arerequired to maintain the silentstate: the nucleosomes are

typically underacetylatedand methylated on lysine 9 ofhistone H3 (H3K9me), whichcreates a binding site forchromo-domain proteins suchas Swi6 (HP1).

An elegant series of studies hasshown that the heterochromaticrepeats are transcribed by RNApolymerase II and that these

transcripts themselves areprocessed by Dicer, a componentof the RNA interference (RNAi)machinery, into short-interfering(si)RNAs. The production ofsiRNAs is essential for targetingthe ‘RNA-induced initiation oftranscriptional gene silencing’(RITS) complex — composedof Ago1, Chp1 andTas3 — to heterochromatinrepeats. This in turn leads to therecruitment of the histonemethyltransferase Clr4. Theconsequent methylation of H3 onlysine 9 by Clr4 allows binding ofthe chromo-domain proteinsSwi6 and Chp1, forminga nucleation site from whichheterochromatin can spreadoutwards along the chromatinfibre [1].

Cells need to restrictheterochromatin to specificdomains in order to avoidrepression of essential genes. Buthow is the silencing machinerytargeted solely to specific loci?And how is heterochromatincontained and prevented fromspreading into other regions of thegenome? One possibility is thatcomponents of heterochromatinrecognize and bind specificsequences within theheterochromatic domains that areabsent in euchromatin. However,this does not explain howa euchromatic marker gene issilenced when it is placed insidea block of heterochromatin.Another possibility is that specificboundary elements are located atthe borders betweenheterochromatin and euchromatin.These elements might act asbuffers to impede the spreading ofheterochromatin to neighbouringchromatin. A third possibility isthat specific factors act as‘anti-silencers’. Such proteinsmight antagonize RNAi-mediatedheterochromatin assembly atparticular steps in the pathway.The balance between ‘silencer’and ‘anti-silencer’ activities mightensure the normal distribution ofheterochromatin and euchromatindomains. Perturbations couldenhance or reduce the formationof silent chromatin.

Several recent papers [2–5]report evidence that these lasttwo mechanisms operate in

DispatchR637

S. pombe. Two of the new studies[2,3] demonstrate the existenceof chromatin boundariessurrounding heterochromatic lociin fission yeast. Transfer (t)RNAgenes and B-box motifs werefound to be functionalcomponents of these boundaryelements and their activityprevents heterochromatin marksfrom oozing out into surroundingdomains (Figure 1A,B). Otheranalyses suggest that, in additionto boundary elements, ‘anti-silencer’ factors play an importantrole in the negative regulation ofheterochromatin. In particular, ithas been shown that Epe1,a JmjC domain protein,counteracts repressive chromatinby facilitating the recruitment ofRNA polymerase II toheterochromatic loci via Swi6(Figure 1A,B) [4].

As reported recently in CurrentBiology, Iida et al. [5] have shownthat the fission yeast orthologue ofthe Caenorhabditis elegans geneEnhancer of RNA Interference 1(eri1) has ‘anti-silencer’ activity.The worm protein ERI-1 wasinitially shown to be a nucleasethat can degrade siRNAs in vitro,and it was suggested that it mightdiminish the pool of active siRNAsin the cells [6]. Consistent with this,worms lacking ERI-1 displayenhanced RNAi silencing [6]. Iidaet al. [5] showed that S. pombe Eri1binds to and degradesdouble-stranded RNA in vitro.Mutation of Eri1’s catalytic domainleads to increased levels ofcentromeric siRNAs which areassociated with RITS complexes.Although cells lacking Eri1display no change in the levelsof silent chromatin modificationover centromeric repeats, H3K9methylation and the silencingof marker genes inserted inthese repeats are noticeablyincreased, suggesting that theformation of heterochromatin viaRNAi is enhanced on markergenes [5].

This role for Eri1 in opposingsilencing is reinforced by anotherrecent study [7] in which theTas3 component of RITS wasartificially tethered to ura4 mRNA.The ura4+ gene of fission yeastis located in euchromatin andis normally constitutively

expressed. However, coercingthe recruitment of RITS to theura4 transcript resulted insilencing of ura4 expression ina manner that is dependent onRNAi, H3K9 methylation andSwi6. Thus, diverting the RNAimachinery to a transcript cantrigger siRNA synthesis,silencing and heterochromatinformation on homologouschromatin.

Surprisingly, despite the factthat siRNA homologous to the ura4transcript are found within theRITS effector complex, a secondcopy or ura4+ at a distinct locationin the genome is not silencedunless the Eri1 nuclease is alsoabsent (Figure 1C,D). In mostsystems the RNAi machineryhomes in on target RNAs bycomplementarity with the siRNAsborne by the RISC effectorcomplex. Yet it seems that infission yeast RNAi is constrained,so that unlike in otherorganisms it is unable to silenceidentical sequences in thegenome. The reasons for, andmechanism of, this restrictedform of RNAi are unknown butit is clear that Eri1 contributesto it [7].

But how does Eri1 exert itsnegative influence on RNAi? It hasbeen suggested that Eri1 mightdegrade siRNAs or theendogenous non-codingtranscripts involved in triggeringRNAi. A different scenario issupported by two recentpublications [8,9] that show thatEri1 is required for RNAi activityagainst several endogenoussomatic genes in C. elegans.These observations suggest thatEri1’s negative effect on RNAi maybe a consequence of competitionfor resources of this pathway, asEri1 stimulates siRNA productionagainst those genes, which in turndiminishes the intensity of RNAiresponse to other stimuli [8,9].Applying the same reasoning tofission yeast, it is possible thatRNAi might have anotherunknown regulatory role in whichEri1 is a central player. Indeed Iidaet al. [5] observed thatoverexpressing Eri1 is toxic to thecells, a fact that cannot be simplyexplained by the loss ofheterochromatin or RNAi, as none

of these functions is essential inthis organism. Although theauthors suggest that toxicity maybe due to this unspecific nucleaseactivity affecting the stability ofother cellular RNAs, high Eri1levels might instead causeexcessive degradation ofspecific target RNAs, whichin turn would compromise cellgrowth.

Taken together these newreports suggest that different,parallel mechanisms restrictheterochromatin to specificdomains. Heterochromatin is notessential in fission yeast but weexpect that an excess of it mightbe deleterious to the cell.Surprisingly, loss of Eri1 or Epe1has no apparent affect on cellviability [3,4]. In a way, this couldmean that the ‘anti-silencers’ arestemming a trickle rather thana flood — the cell’s capacity toassemble more heterochromatinmay well be limited due to lowlevels of key proteins such asSwi6. On the other hand, the cellmay possess other undiscovered‘anti-silencers’ that actredundantly with Eri1. All shouldfall in place once it is clarifiedhow the different anti-silencers,such as Eri1 and Epe1, togetherwith boundary elementsnegatively regulateheterochromatin formation andwhether they cooperate with eachother.

References1. Martienssen, R.A., Zaratiegui, M., and

Goto, D.B. (2005). RNA interferenceand heterochromatin in the fissionyeast Schizosaccharomycespombe. Trends Genet. 21,450–456.

2. Noma, K., Cam, H.P., Maraia, R.J., andGrewal, S.I. (2006). A role for TFIIICtranscription factor complex ingenome organization. Cell 125,859–872.

3. Scott, K.C., Merrett, S.L., and Willard, H.F.(2006). A heterochromatin barrier partitionsthe fission yeast centromere into discretechromatin domains. Curr. Biol. 16,119–129.

4. Zofall, M., and Grewal, S.I. (2006).Swi6/HP1 recruits a JmjC domainprotein to facilitate transcription ofheterochromatic repeats. Mol. Cell 22,681–692.

5. Iida, T., Kawaguchi, R., and Nakayama, J.(2006). Conserved ribonuclease, Eri1,negatively regulates heterochromatinassembly in fission yeast. Curr. Biol. 16,1459–1464.

6. Kennedy, S., Wang, D., and Ruvkun, G.(2004). A conserved siRNA-degradingRNase negatively regulates RNAinterference in C. elegans. Nature 427,645–649.

Current Biology Vol 16 No 16R638

7. Buhler, M., Verdel, A., and Moazed, D.(2006). Tethering RITS to a nascenttranscript initiates RNAi- andheterochromatin-dependentgene silencing. Cell 125, 873–886.

8. Duchaine, T.F., Wohlschlegel, J.A.,Kennedy, S., Bei, Y., Conte, D., Jr.,Pang, K., Brownell, D.R., Harding, S.,Mitani, S., Ruvkun, G., et al. (2006).

Ocean Ecology:

New research that combines ocepredict population structure of cotropical reef ecosystems.

Simon R. Thorrold

The precarious future of coral reefsthroughout the world’s tropicaloceans has generatedunprecedented interest in the useof marine protected areas (MPAs)to conserve these unique habitats[1,2]. Occasionally it is possible toconserve an entire ecosystem, ashas recently been proposed for theNorthwestern Hawaiian Islands,but more commonly a number ofsmaller areas are designated forvarying levels of protection. Butwhich areas should be designatedfor MPAs, and where shouldfishing or other extractive activitiesbe allowed? Satisfying answers to

Figure 1. Ocean circulation models aretion connectivity during the pelagic larv

The models allow for visualization of comdistribution of early stage virtual larvaelarvae (red dots) released from historicsynagris) around Cuba. (Image courtesy

Functional proteomics reveals thebiochemical niche of C. elegans DCR-1 inmultiple small-RNA-mediated pathways.Cell 124, 343–354.

9. Lee, R.C., Hammell, C.M., and Ambros, V.(2006). Interacting endogenous andexogenous RNAi pathways inCaenorhabditis elegans. RNA 12,589–597.

Don’t Fence Me in

an circulation and genetic models torals will help conservation efforts in

this question has flummoxedmarine ecologists because itdepends critically upon someknowledge of dispersal distances(connectivity) in populations ofreef organisms (Figure 1). As theyreport in this issue of CurrentBiology, Galindo, Olson andPalumbi [3] used anoceanographic model to generatea larval connectivity matrix amongalmost 100 reef sites in theCaribbean region. The matrix wasthen used to estimate gene flowamong the locations in a simplegenetic model that incorporatedlife history characteristics ofreef-building coral. Modelpredictions matched well with

being used increasingly to determine popula-al phase of marine fish and invertebrates.

plex dispersal patterns — in this instance the(yellow dots) and 30-day old late stage virtualal spawning sites of lane snapper (Lutjanusof Claire Paris, University of Miami.)

Wellcome Trust Centre for Cell Biology,6.34 Swann Building, King’s Buildings,University of Edinburgh, Edinburgh EH93JR, UK.E-mail: robin.allshire@ed.ac.uk

DOI: 10.1016/j.cub.2006.07.033

empirical data on genetic variationin Caribbean corals, suggestingthat the ocean circulation modelprovides a reasonable facsimile ofrealized larval dispersal.

Biodiversity in the ocean realm,as in terrestrial environs, isgenerated and maintained bybarriers to dispersal. But while it isintuitively obvious that mountainranges act to constrict animalmovements on land, physicalbarriers in the ocean are muchmore difficult for humans todiscern. A further complicationarises because dispersal of mostcoral reef fish and invertebratesoccurs primarily during a relativelyshort pelagic larval phase. Oncepelagic, larvae are subject todiffusion, turbulence andadvection in oceanic watermasses that can potentially lead todispersal of hundreds ofkilometers [4]. But it has provedextremely difficult to eithermeasure the frequency with whichlong distance movements duringthe larval phase occur, oralternatively to identify dispersalbarriers that may act to isolatepopulations over ecological orevolutionary time. Data onecological connectivity is critical,however, for spatial managementof fisheries and the control ofinvasive species, while gene flowover evolutionary time scales willdetermine genetic structure andpatterns of biodiversity in marineecosystems.

Marine invertebrate and fishlarvae are notoriously difficult totrack in the field because they areinvariably tiny and are quicklydiluted in vast volumes of water [5].Instead, Galindo et al. [3] tackledthe problem by followingparticles — ‘virtual larvae’ — inCaribbean Sea currents derivedfrom the Miami IsopycnalCoordinate Ocean Model(MICOM). Particles were deemed