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to give a nucleus with 114 protons and 173neutrons, which falls into slightly deeperwater off the island. So far there have beentwo events. But the beauty of this experimentis that the decay properties of the new isotopecould be calculated from the observed prop-erties of the first isotope of element 114. Theprediction of a single a-decay followed byspontaneous fission is confirmed convinc-ingly3.

In the latest LBNL experiment2, the pre-vious philosophy of using a 208Pb target wasadopted. This nuclide has a closed shell ofneutrons (N 4 126) and of protons (Z 4 82)producing an unusually stable nucleus (seeBox 1). The extra binding energy of thisdouble-closed-shell system leads to a coolercompound nucleus that needs to evaporateonly one neutron to survive fission. A projec-tile with 36 protons (86Kr) enabled the groupto leapfrog element 114 and reach Z 4 118(seen in three events), which then decays to Z4 116, 114 and so on. In terms of the ques-

tion “Just how many stable elements is it pos-sible to make?”, this increases the maximumatomic number by a further four units. But,for the isotope of Z 4 114 observed in thelong Dubna decay chain (Fig. 2), the lifetimeis over four orders of magnitude greater thanthat for the Z 4 114 isotope in the LBNLchain. Similar comparisons hold for Z 4112 and Z 4 110. Even the 114 isotope in theshort Dubna decay chain (Fig. 2) has a life-time enhanced by over three orders of mag-nitude. So, in terms of reaching the island ofstability, the Dubna experiments appear sofar to be the closest.Neil Rowley is at the Institut de RecherchesSubatomiques, 23 rue du Loess, F-67037, StrasbourgCedex 2, France.e-mail: Neil.Rowley@ires.in2p3.fr1. Oganessian, Yu. Ts. et al. Phys. Rev. Lett. (submitted).

2. Ninov, V. et al. Phys. Rev. Lett. (submitted).

3. Oganessian, Yu. Ts. et al. Nature 400, 242–245 (1999).

4. Hofmann, S. in Proc. VI Int. School-Seminar on Heavy Ion

Physics, Dubna, September 1997 (eds Oganessian, Yu. Ts. &

Kalpakchieva, R.) 385 (World Scientific, Singapore, 1998).

sexual dimorphism in the EOD of somegymnotiforms.

Stoddard presents both correlational andexperimental evidence that predation canfavour the use of biphasic signals. One canchange a monophasic EOD to a biphasic oneby adding a negative-going second phase,which shifts the frequency upwards (Fig. 1).All electrolocating fish have ampullaryorgans, which are extremely sensitive to lowfrequencies and excel at detecting the weakelectric fields of prey. But these receptors areless sensitive to the higher frequencies of thebiphasic EODs that many gymnotiforms usein communication (Fig. 1). Gymnotiformsalso evolved a second set of electroreceptors,tuberous organs, which are less sensitivethan ampullary organs but are tuned to thehigher frequency of the EOD. So both thesignal and the receiver in the gymnotiformcommunication system operate in a fre-quency range above that to which ampullaryorgans are most sensitive. It would seem thatsuch a frequency shift would reduce preda-tion risk.

To test this hypothesis, Stoddard and hisgraduate student Marina Olman trained anelectric eel, a predator, to respond to electri-cal discharges; the reward was associatedwith approach to either a monophasic orbiphasic EOD. The predator was more likelyto approach the monophasic pulse. Theseresults suggest that there is an advantageto producing biphasic pulses, but do not

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NATURE | VOL 400 | 15 JULY 1999 | www.nature.com 211

Behavioural ecology

Electrifying diversityMichael J. Ryan

Sexual selection often favours signalsthat are conspicuous; the more con-spicuous the signal, the more attrac-

tive the signaller is to mates1. But conspicu-ousness incurs a cost because predators caneavesdrop; the more conspicuous the signal,the more risky it is. So natural selection gen-erated by predation is often viewed as a con-straining force in signal evolution. In the faceof predation, for example, crickets evolvenon-calling strategies, guppies evolve dullcolours, and túngara frogs produce less con-spicuous calls1. In a study described on page254 of this issue2, however, Philip Stoddardargues that predation by electrolocatingpredators on gymnotiform electric fish hasbeen a creative rather than a constrainingforce on the evolution of electric-organ dis-charges (EODs).

There are more than 100 species of gym-notiforms, or knife fish, in the fresh waters ofCentral and South America. These animalsare nocturnal, and often live in murky waterswhere visual communication would be diffi-cult even in the daytime. But poor visibilityhas little effect on them, as they rely on theirability to produce and detect weak electricalfields for sensing their environment as wellas for communicating with one another. TheEODs, however, make the fish vulnerable toelectropredators such as electric eels andcatfish.

It seems that the ancestral EOD was anintermittent monophasic pulse. But manygymnotiforms produce a biphasic EOD.What forces might favour the evolution ofsuch a signal? Stoddard addresses three al-ternative hypotheses: electrolocation, sexual

selection and predator avoidance. He arguesthat predator avoidance was the initial forcefavouring the evolution of the complexEODs, although sexual selection might havethen been responsible for the subsequent

Figure 1 Signalling in electric fish. The waveform of a monophasic (a) and biphasic (c) electric-organdischarge (EOD) with the corresponding power spectra (monophasic, b; biphasic, d). The arrowsshow the sensitivity of two types of electrosensitive predators, catfish at about 8 Hz (blue) andgymnotiforms at about 30 Hz (red). The biphasic EOD is from Brachypopomus pinnicaudatus,gymnotiform prey; the monophasic waveform is that same waveform with the negative componentdeleted. The figures are modified from Figs 3c and 3d of Stoddard2, who argues that predation hasfavoured an increase in the complexity of EODs because the biphasic signals are less detectable bypredators than are the monophasic signals.

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explain why three species of gymnotiformstill produce monophasic EODs. These,Stoddard argues, might be the exceptionsthat prove the rule. Of the three monophasicspecies, one is an electropredator, one lives inan area devoid of electropredators, and oneproduces an EOD which resembles that of anelectric eel.

This study describes a convincing way inwhich predation may have promoted ratherthan constrained signal diversity. But it isnot a unique case, as predation is known tohave had similar effects in other systems. Itcaused moths to evolve ears to detect, andsignals to deter, bat predation; these traitswere then co-opted for communication,resulting in males that communicate theirpresence to females with ultrasonics (insome species, males and females even con-duct an ultrasonic duet)3. Also, it has beensuggested that offspring might evolve sig-nals that are more conspicuous to predatorsin order to manipulate parental behaviour4;bird nestlings giving loud, conspicuousbegging calls, and children holding theirbreath in parental defiance, are two exam-ples.

Stoddard’s study gives us a glimpse intothe complicated world of signal evolution ofone system; a more general understanding,however, is far off. Consider Zuk and Kollu-ru’s5 review of the predation costs of sexualsignals. They pointed out that there aremany more examples of predators attractedto signals in the acoustic mode than in thevisual mode (electrical communication ismore similar to acoustic than visual com-munication). This bias is probably becauseit is easier to study acoustic than visual com-munication. Nevertheless, it is crucial toknow how predator effects on communica-tion systems might vary among sensorymodalities.

For example, is it as likely that potentialprey can evolve electrical (say, biphasic puls-es) or acoustic (say ultra- or subsonic) sig-nals out of the range of their predators thanit is for prey to evolve visual signals (say inthe ultraviolet) to escape predators in thatmodality? One part of the answer mightdepend on the lability of signals in a givenmodality. Another must derive from thepredator’s receiving systems. Do thedemands of communication on a sensorysystem constrain the uses of that system inother tasks, and does this vary among senso-ry modalities? For example, does tuning anelectroreceptive or auditory system to onetype of signal, a weak electric field or anecholocation call, constrain this system frombeing used to locate prey making very differ-ent types of sounds? It might be so in electriceels, but appears not to be in frog-eatingbats6.

Also, more generally, we can ask howconstrained different sensory systems are intheir ability to evolve. Can we compare the

changes in the inner ear of a vertebrate, need-ed to allow that animal access to ultrasonicemissions made by its prey, to changes in theretina of the same animal that would give itaccess to ultraviolet signals of different prey?Probably not. Only studies of the entirebiology of communication systems canallow an appreciation of their diversity — anargument that provides strong support forthe kind of integrative approach taken byStoddard.

Michael J. Ryan is in the Section of IntegrativeBiology, University of Texas, Austin, Texas 78712,USA.e-mail: mryan@mail.utexas.edu1. Andersson, M. Sexual Selection (Princeton Univ. Press, 1994).2. Stoddard, P. K. Nature 400, 254–256 (1999). 3. Simmons, R. B. & Conner, W. E. J. Insect Behav. 9, 909–919

(1996).4. Zahavi, A. & Zahavi, A. The Handicap Principle: A Missing Piece

of Darwin’s Puzzle (Oxford Univ. Press, 1997).5. Zuk, M. & Kolluru, G. R. Q. Rev. Biol. 73, 415–438

(1998).6. Tuttle, M. D. & Ryan, M. J. Science 214, 677–678 (1981).

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NATURE | VOL 400 | 15 JULY 1999 | www.nature.com 213

Signal transduction

Neither straight nor narrowMark Peifer

Back when I was a boy, things were sim-pler. Web browsers fancied spiders, cellphones were used by prisoners to call

their lawyers, and signal transduction — themechanism by which information is trans-ferred from the surface of a cell to its nucleus— proceeded though a linear series of simplesteps. But times have changed, and fivepapers in Nature1–5 (the latest of which arefound on pages 271, 276 and 281 of thisissue) provide a dramatic example of this.The discovery of new components and con-nections is converting the stepwise, linearpathways of information transfer intoincreasingly complex networks.

Most of our cells do not act in isolation —rather, they respond to signals from theirneighbours. Much of the cellular machineryis devoted to receiving these signals and thentransducing them, relaying information tothe components that mediate the cell’sresponse. In the simplest view, these signal-transduction pathways are envisaged aslinear wiring diagrams, like telephone linesthat link individual customers to the phone company.

The decisions that cells make are domi-nated by just a few families of cell–cell sig-nals. Among these are members of theWingless signal-transduction pathway,inappropriate activation of which con-tributes to human cancers. (On a lighternote, this pathway may also offer a cure forbaldness6.) The genes required for Winglesssignalling were first identified in the fruitflyDrosophila melanogaster (and, for simplici-ty, only the Drosophila names of compo-nents in the pathway are mentioned here).The pathway initially seemed simple andlinear (Fig. 1; and reviewed in ref. 7). A pro-tein called Armadillo is the key regulatedcomponent. Normally, Armadillo is unsta-ble inside cells because it is targeted fordestruction by a kinase known as Zeste-white3 (Zw3). This kinase is somehowcounteracted by another protein, Dishev-elled, which is activated when Winglessbinds at the cell surface. The receptors forWingless signals are members of the Frizzled

protein family, distant relatives of guanine-nucleotide-binding (G)-protein coupledreceptors. So, when Wingless binds to Friz-zled receptors, Dishevelled is activated,somehow counteracting Zw3 and stabilizingArmadillo. Armadillo then enters the nucle-us, where it interacts with transcriptionfactors and activates Wingless-responsivegenes.

But this simple, linear picture haschanged dramatically — additional regula-tory inputs have been discovered at each levelin the pathway. There are, for example, manyreceptors in the Frizzled family, as well asmany Wingless ligands, and we are only justbeginning to discover how these proteins canbe mixed and matched. Moreover, secretedantagonists of Wingless (a subset of whichare secreted analogues of Frizzled receptors),negatively regulate signalling (reviewed inref. 7). The papers by Tsuda et al.2 and Linand Perrimon3 further complicate the issue,because they suggest that the Winglessreceptor is, in fact, a protein complex, with

Figure 1 Our humble beginnings — early ideasabout the Wingless signalling pathway. Initiallythis pathway was thought to be a simple, linearcascade. Binding of Wingless to its receptorleads to activation of Dishevelled, whichcounteracts the repressive effects of the Zeste-white3 (Zw3) kinase and allows expression ofArmadillo. After crossing into the nucleus,Armadillo can then activate Wingless-responsivegenes.

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