Social Learning: Ants and the Meaning of Teaching

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  • Dispatchooctye, with a volumew25 000times larger than that of a typicalsomatic cell. Intriguingly, a recentultrastructural study [20] 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 [19] 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. [1]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 [13].Surprisingly, however, convincingdemonstrations of teachingbehaviour in animals are rare.

    Caro and Hauser [4] 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: jan.ellenberg@embl.de

    DOI: 10.1016/j.cub.2006.03.081

    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 [6]. 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 [7]). 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 [8] 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 [9]. 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 [8] 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

    1

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    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

    e

    LeaderFollower

    Current Biology

    3

    F

    albipennis ants.

    -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) [8]. Oncefollower re-establishes antennal contact,and Hauser [4]. 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