Dispatchooctye, with a volumew25 000times larger than that of a typicalsomatic cell. Intriguingly, a recentultrastructural study  of isolatedXenopus oocyte nuclei observedfilaments, which could bedecorated with anti-actinantibodies and which weresensitive to actin depolymerizingdrugs, connecting nuclear porecomplexes to intranuclearstructures like nucleoli.
changes in consistency of oocytenucleoplasm of the newt Pleurodeleswaltlii. J. Cell Biol. 88, 410421.
5. Roeder, A.D., and Gard, D.L. (1994).Confocal microscopy of F-actindistribution in Xenopus oocytes. Zygote 2,111124.
6. Parfenov, V.N., Davis, D.S., Pochukalina,G.N., Sample, C.E., Bugaeva, E.A., andMurti, K.G. (1995). Nuclear actin filamentsand their topological changes in frogoocytes. Exp. Cell Res. 217, 385394.
7. Clark, T.G., and Rosenbaum, J.L. (1979).An actin filament matrix in hand-isolatednuclei of X. laevis oocytes. Cell 18,11011108.
8. Merriam, R.W., and Hill, R.J. (1976). Theherpes virus capsids  can beinhibited by the presence ofnon-polymerizable actin ordepolymerization of F-actin.
It is unclear from these studiesjust how direct the requirement foractin in transport within nuclei is,but it is reasonable to suppose thatdirected transport would beimportant in a massive nucleussuch as that of an amphibian
R323We are just beginning tounderstand forms and functions ofnuclear actin. Bohnsack et al. have unraveled why actin isallowed in nuclei of Xenopusoocytes and showed that it canform a crosslinked filamentousstructure in them. It remains to beshown, however, which fibrousactin structures can be found innuclei of different cells in vivo andwhat their molecular functionsare exciting questions for futureresearch.
Social Learning: AMeaning of Teach
Recent research on ants shows thatfunction of teaching nave ants aboutnew experiments represent perhapsteaching in animals to date, the finditeaching formally differs from other
Ellouise Leadbeater,Nigel E. Raine and Lars Chittka
Learning from others is sofundamental to humans that weactively speed up the sociallearning process we teach.Non-human animals can also learnfrom members of their own species,and they might be expected toaccrue considerable inclusivefitness benefits by coaching kin toReferences1. Bohnsack, M.T., Stuven, T., Kuhn, C.,
Cordes, V.C., and Gorlich, D. (2006). Aselective block of nuclear actin exportstabilizes the giant nuclei of Xenopusoocytes. Nat. Cell Biol. 8, 257263.
2. Stuven, T., Hartmann, E., and Gorlich, D.(2003). Exportin 6: a novel nuclear exportreceptor that is specific for profilin.actincomplexes. EMBO J. 22, 59285940.
3. Clark, T.G., and Merriam, R.W. (1977).Diffusible and bound actin nuclei ofXenopus laevis oocytes. Cell 12, 883891.
4. Gounon, P., and Karsenti, E. (1981).Involvement of contractile proteins in thegerminal vesicle nucleus of Xenopuslaevis oocytes as a selective storagereceptacle for proteins. J. Cell Biol. 69,659668.
9. Callan, H.G., and Lloyd, L. (1960).Lampbrush chromosomes of crestednewts Triturus cristatus (Laurenti). Phil.Trans. Roy. Soc. B 243, 135219.
10. Gall, J.G. (1952). The lampbrushchromosomes of Triturus viridescens.Exp. Cell Res. Suppl. 2, 95102.
11. Gall, J.G. (2006). Exporting actin. Nat. CellBiol. 8, 205207.
12. Wasser, M., and Chia, W. (2000). TheEAST protein of Drosophila controls anexpandable nuclear endoskeleton. Nat.Cell Biol. 2, 268275.
13. Lenart, P., Bacher, C.P., Daigle, N., Hand,A.R., Eils, R., Terasaki, M., and Ellenberg,
nts and theing
running in tandem might serve thethe path to a target. Although thesethe most highly controlled study ofngs prompt the question of howforms of communication.
facilitate the rapid development ofadaptive behaviour .Surprisingly, however, convincingdemonstrations of teachingbehaviour in animals are rare.
Caro and Hauser  laid out thefollowing minimum criteria forinformation transfer betweenanimals to be classified asteaching. The animal that conveysinformation must incur a cost, or atleast not reap an immediate benefitJ. (2005). A contractile nuclear actinnetwork drives chromosomecongression in oocytes. Nature 436,812818.
14. Ryabova, L.V., Betina, M.I., andVassetzky, S.G. (1986). Influence ofcytochalasin B on oocyte maturation inXenopus laevis. Cell Differ. 19, 8996.
15. Gard, D.L., Cha, B.J., and Roeder, A.D.(1995). F-actin is required for spindleanchoring and rotation in Xenopusoocytes: a re-examination of the effects ofcytochalasin B on oocyte maturation.Zygote 3, 1726.
16. Holaska, J.M., Kowalski, A.K., and Wilson,K.L. (2004). Emerin caps the pointed endof actin filaments: evidence for an actincortical network at the nuclear innermembrane. PLoS Biol. 2, E231.
17. Carmo-Fonseca, M., Platani, M., andSwedlow, J.R. (2002). Macromolecularmobility inside the cell nucleus. TrendsCell Biol. 12, 491495.
18. Chuang, C.H., Carpenter, A.E., Fuchsova,B., Johnson, T., de Lanerolle, P., andBelmont, A.S. (2006). Long-rangedirectional movement of an interphasechromosome site. Curr. Biol. 16, 825831.
19. Forest, T., Barnard, S., and Baines, J.D.(2005). Active intranuclear movement ofherpesvirus capsids. Nat. Cell Biol. 7,429431.
20. Kiseleva, E., Drummond, S.P., Goldberg,
M.W., Rutherford, S.A., Allen, T.D., andWilson, K.L. (2004). Actin- and protein-4.1-containing filaments link nuclear porecomplexes to subnuclear organelles inXenopus oocyte nuclei. J. Cell Sci. 117,24812490.
Gene Expression and Cell Biology/Biophysics Units, European MolecularBiology Laboratory (EMBL),Meyerhofstrasse 1, D-69117 Heidelberg,Germany.E-mail: firstname.lastname@example.org
from the subsequently alteredbehaviour of the receiver. Thecandidate behaviour has to beperformed only when uninformedindividuals are present. Hence,although juvenile songbirds learntheir songs by listening to adultmales, the adult is not teachingbecause he will sing irrespective ofthe youngsters presence. Finally,the teaching must lead the pupil tolearn a skill, or acquire knowledgethat it would not otherwise obtain,or at least that it would take longerto acquire.
Perhaps the most convincingcandidates for teaching amongvertebrates involve carnivoreslearning to hunt (reviewed in [4,5]).Mother cheetahs that wouldnormally capture and kill preywithout delay bring live prey backto the nest when their cubs are very
Current Biology Vol 16 No 9young. Prey is killed by the motherin front of the cubs. Later, when thecubs begin accompanying her onhunting trips, the mother releasesprey in front of them, which thecubs attempt to catch, sometimesat the cost of losing the preyaltogether . The cubs predatoryskills improve over this period,although it remains to be shownthat this results directly from suchpractice (the same applies ina study on domestic cats ). Otherpotential cases of teaching involvechimpanzees learning to use stonehammers and anvils, and ospreysteaching their offspring to snatchfish from the water [4,5], but as yetthese rely only upon weakanecdotal evidence.
In contrast, Franks andRichardsons  well-controlledstudy on tandem-runningTemnothorax ants was carried outin a laboratory. The intimateinteraction between leader andfollower in a pair of tandemlyrunning ants at first sight bears allthe hallmarks of a parent teachinga child to ride a bicycle. An
nave nest mates to newlydiscovered food sources or nestingsites, stopping if the follower losesregular antennal contact . Whenthe pair becomes separated, asoccurs when the follower makeslooping movements possiblysearching for landmarks, the leaderremains still, only continuingtowards the food when the followerhas completed her exploratorycircuit (Figure 1). Franks andRichardson  demonstrate thatthere are clear two-wayinteractions between thetandem-running ants. When thegap between them becomes toolarge, and antennal contactbetween the pair is lost, the leaderslows down and the followeraccelerates to catch up. Thisbidirectional feedback loopappears to maximise the speed atwhich the two can progress, whileallowing the follower to memorisethe path and its surroundinglandmark features.
Such tandem-running meetsmost of the criteria for teaching setout in the definition given by Caro
the leader continues onwards towards the food. If contact between follower and leaderbecomes less frequent during a tandem-run, the leader will slow down to allow the fol-lower to catch up (point 2).01
Figure 1. Tandem-running by Temnothorax
(A) Schematic view of path taken by a tandemants from their nest (N) to a food source (F).follower (blue line) during the same tandemthe food source, whilst followers are nave ofthe food source (red path) so long as the follocontact with the leaders legs or abdomen.frequent periods when the leader remains scircuit, possibly to memorise landmarks althis exploratory circuit is complete, and the
R324experienced ant will lead individual2 3
-running pair of Temnothorax albipennis(B) Running speed of leader (red line) and-run. Tandem leaders have experience ofits location. The leader proceeds towardswer (blue path) maintains regular antennalProgress of the tandem pair is slowed bytill whilst the follower performs a loopedong the path (points 1 and 3) . Oncefollower re-establishes antennal contact,and Hauser . When alone, theleader does not incorporate thefrequent pauses which are used bythe follower to perform orientationloops. Hence the leadersbehaviour is clearly modified in thepresence of a nave observer.Leaders incur a time cost: whenan experienced forager is notleading a follower, she travelsfaster to the food source anddoes not stop en route . Asa result, the follower (pupil) findsthe target more quickly than shewould do if searching for it alone.While it appears likely thatfollowers learn route-specificinformation duringtandem-running, it remains tobe shown empirically preciselywhat information is obtained.
Franks and Richardson  refineCaro and Hausers  workingdefinition of teaching byintroducing an additional criterion:that feedback from the learner tothe experienced individual mustbe demonstrated. Suchfeedback clearly distinguishestandem-running from other formsof signalling in ants, such asscent-marking food sources, orreleasing alarm pheromones inthe presence of nest intruders .In these cases, both the signaland the response are largelyhard-wired; and there is no needto assume that learnt informationhas been transmitted, nor is therea need to invoke learning toexplain the receivers response.Most simple forms of signalling,such as use of pheromones, do notappear to meet several criteria laidout by Caro and Hausers teachingdefinition: such signals aredisplayed irrespective of thepresence of a nave receiver, anddo not lead to the long lastingchanges of receiver behaviourthat would qualify as learning[10,11]. So the additional criterionof feedback from the taughtindividual seems unnecessary.Responding to feedback frompupils makes for more efficientteaching, but teaching, albeitperhaps at a lower quality, can stilloccur in the absence of suchfeedback.
In contrast, tandem-running inants, just like dancing inhoneybees, is a much moreadvanced form of communication.These behaviours specifically
transmit learnt knowledge withflexible information content: in thehoneybee dance, for example, anylocation within the flight range ofthe colony can be encoded. Theacquired information cansubsequently be used by newlyinformed individuals in a mannerthat is temporally and, in thecase of a honeybee dance,spatially separated from theinformation transfer event(Figure 2). This underlines thenotion that invertebrates, despitetheir often miniscule brains, mightnot be fundamentally different fromvertebrates in the types ofinformation processing of whichthey are capable , perhaps thedifference is just in the amount ofinformation that can be stored andprocessed in parallel.
But however impressive theseinsect forms of social learning maybe, we argue that they do notconstitute forms of teaching. Ourreservations relate to the types ofinformation that are beingcommunicated. Tandem-runningants and dancing bees transferinformation about a location ofinterest. While the mode ofinformation transfer is different, thecontent is equivalent to humansinforming each other about thelocation of a good restaurant: youtell, not teach, someone itslocation. In a similar vein, parentshelping their children withmathematics homework couldsimply tell them the answer. Buta parent might also teach the childhow to work out the solution, ratherthan to simply tell them what it is.Felids that teach their offspring tohunt facilitate the learning of anability to perform actions a skill.In more formal terms, we suggestthat teaching should be reservedfor transfer of skills, concepts,rules and strategies not simplythe handing over of declarativeinformation (facts), or simpleprocedural information (such ashow to get to a place, by guidingother individuals there).
Caro and Hausers  definitionclassifies both types of behaviouras teaching. Nonetheless, the twohave different functionalconsequences. Transferring basicinformation is a solution toa problem in one context, but
DispatchR325teaching a skill allows the recipientto solve the problem in multiplesituations. When describingteaching in humans we sometimesfail to differentiate; a historyteacher may tell a pupil a fact, suchas when a war took place, and stillbe said to be teaching. Whenconsidering the evolution ofteaching behaviour, however,rigorous terminology allows us tounderstand differences in theadaptive benefits that transferringknowledge and transferring skillsmay afford: thus it appears usefulto reserve distinct terms for distincttypes of information exchangebetween animals.
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3. Chittka, L., and Leadbeater, E. (2005).Social learning: public informationin insects. Curr. Biol. 15,R869R871.
4. Caro, T.M., and Hauser, M.D. (1992). Isthere teaching in nonhuman animals?
5. Shettleworth, S.J. (1998). Cognition,Evolution, and Behavior (Oxford: OxfordUniversity Press).
6. Caro, T.M. (1992). Cheetahs of theSerengeti Plains: Grouping in AsocialSpecies (Chicago: University of ChicagoPress).
7. Caro, T.M. (1980). Predatory behaviour indomestic cat mothers. Behaviour 74,128148.
8. Franks, N.R., and Richardson, T. (2006).Teaching in tandem-running ants. Nature439, 153.
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13. Frisch, K.v. (1967). The Dance Languageand Orientation of Bees (Cambridge,Massachusetts: Harvard University Press).
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School of Biological and ChemicalSciences, Queen Mary University ofLondon, Mile End Road, London E1 4NS,UK.E-mail: email@example.com
rected information transfer, we suggest this does not represent true teaching: thedancer is telling, rather than teaching, the recruits where to go to find food. (Photoby Scott Camazine.)Figure 2. Honeybee waggle dancer surroun
Successful honeybee foragers use a ritualisconvey distance and direction informationdarkness of the hive [13,14]. The dancer traformation content: she communicates theshe herself has learnt. The potential recruitscan subsequently use the information conhive and locate the food source she indicaQ. Rev. Biol. 67, 151174.ded by potential recruits.
ed and abstract communication system toof a food source to their nest mates in thensmits learnt information with a flexible in-location of a profitable foraging site which, shown in a semi-circle behind the dancer,veyed by the dancer when they leave theted. Whilst this is an impressive feat of di-DOI: 10.1016/j.cub.2006.03.078
Social Learning: Ants and the Meaning of TeachingReferences