herpes 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 amphibianooctye, with a volume w25 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.
We 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.
References1. 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, 257–263.
2. Stuven, T., Hartmann, E., and Gorlich, D.(2003). Exportin 6: a novel nuclear exportreceptor that is specific for profilin.actincomplexes. EMBO J. 22, 5928–5940.
3. Clark, T.G., and Merriam, R.W. (1977).Diffusible and bound actin nuclei ofXenopus laevis oocytes. Cell 12, 883–891.
4. Gounon, P., and Karsenti, E. (1981).Involvement of contractile proteins in thechanges in consistency of oocytenucleoplasm of the newt Pleurodeleswaltlii. J. Cell Biol. 88, 410–421.
5. Roeder, A.D., and Gard, D.L. (1994).Confocal microscopy of F-actindistribution in Xenopus oocytes. Zygote 2,111–124.
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, 385–394.
7. Clark, T.G., and Rosenbaum, J.L. (1979).An actin filament matrix in hand-isolatednuclei of X. laevis oocytes. Cell 18,1101–1108.
8. Merriam, R.W., and Hill, R.J. (1976). Thegerminal vesicle nucleus of Xenopuslaevis oocytes as a selective storagereceptacle for proteins. J. Cell Biol. 69,659–668.
9. Callan, H.G., and Lloyd, L. (1960).Lampbrush chromosomes of crestednewts Triturus cristatus (Laurenti). Phil.Trans. Roy. Soc. B 243, 135–219.
10. Gall, J.G. (1952). The lampbrushchromosomes of Triturus viridescens.Exp. Cell Res. Suppl. 2, 95–102.
11. Gall, J.G. (2006). Exporting actin. Nat. CellBiol. 8, 205–207.
12. Wasser, M., and Chia, W. (2000). TheEAST protein of Drosophila controls anexpandable nuclear endoskeleton. Nat.Cell Biol. 2, 268–275.
13. Lenart, P., Bacher, C.P., Daigle, N., Hand,A.R., Eils, R., Terasaki, M., and Ellenberg,
J. (2005). A contractile nuclear actinnetwork drives chromosomecongression in oocytes. Nature 436,812–818.
14. Ryabova, L.V., Betina, M.I., andVassetzky, S.G. (1986). Influence ofcytochalasin B on oocyte maturation inXenopus laevis. Cell Differ. 19, 89–96.
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, 17–26.
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, 491–495.
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, 825–831.
19. Forest, T., Barnard, S., and Baines, J.D.(2005). Active intranuclear movement ofherpesvirus capsids. Nat. Cell Biol. 7,429–431.
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. 117,2481–2490.
Gene Expression and Cell Biology/Biophysics Units, European MolecularBiology Laboratory (EMBL),Meyerhofstrasse 1, D-69117 Heidelberg,Germany.E-mail: [email protected]
DOI: 10.1016/j.cub.2006.03.081
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Social Learning: Ants and theMeaning of Teaching
Recent research on ants shows that running in tandem might serve thefunction of teaching naıve ants about the path to a target. Although thesenew experiments represent perhaps the most highly controlled study ofteaching in animals to date, the findings prompt the question of howteaching formally differs from other forms of communication.
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 to
facilitate the rapid development ofadaptive behaviour [1–3].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 benefit
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
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Figure 1. Tandem-running by Temnothorax albipennis ants.
(A) Schematic view of path taken by a tandem-running pair of Temnothorax albipennisants from their nest (N) to a food source (F). (B) Running speed of leader (red line) andfollower (blue line) during the same tandem-run. Tandem leaders have experience ofthe food source, whilst followers are naıve of its location. The leader proceeds towardsthe food source (red path) so long as the follower (blue path) maintains regular antennalcontact with the leader’s legs or abdomen. Progress of the tandem pair is slowed byfrequent periods when the leader remains still whilst the follower performs a loopedcircuit, possibly to memorise landmarks along the path (points 1 and 3) [8]. Oncethis exploratory circuit is complete, and the follower re-establishes antennal contact,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).
young. 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 andRichardson’s [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. Anexperienced ant will lead individual
naıve 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 Caroand Hauser [4]. When alone, the
leader does not incorporate thefrequent pauses which are used bythe follower to perform orientationloops. Hence the leader’sbehaviour is clearly modified in thepresence of a naıve observer.Leaders incur a time cost: whenan experienced forager is notleading a follower, she travelsfaster to the food source anddoes not stop en route [8]. 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 [8] refineCaro and Hauser’s [4] 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 [9].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 receiver’s response.Most simple forms of signalling,such as use of pheromones, do notappear to meet several criteria laidout by Caro and Hauser’s teachingdefinition: such signals aredisplayed irrespective of thepresence of a naıve 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
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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 [12], 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 Hauser’s [4] definitionclassifies both types of behaviouras teaching. Nonetheless, the twohave different functionalconsequences. Transferring basicinformation is a solution toa problem in one context, butteaching a skill allows the recipient
Figure 2. Honeybee waggle dancer surrounded by potential recruits.
Successful honeybee foragers use a ritualised and abstract communication system toconvey distance and direction information of a food source to their nest mates in thedarkness of the hive [13,14]. The dancer transmits learnt information with a flexible in-formation content: she communicates the location of a profitable foraging site whichshe herself has learnt. The potential recruits, shown in a semi-circle behind the dancer,can subsequently use the information conveyed by the dancer when they leave thehive and locate the food source she indicated. Whilst this is an impressive feat of di-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.)
to 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.
References1. Kendal, R.L., Coolen, I., van Bergen, Y.,
and Laland, K.N. (2005). Trade-offs inthe adaptive use of social and asociallearning. Adv. Stud. Behav. 35,333–379.
2. Galef, B.G., and Giraldeau, L.-A. (2001).Social influences on foraging invertebrates: causal mechanisms andadaptive functions. Anim. Behav. 61,3–15.
3. Chittka, L., and Leadbeater, E. (2005).Social learning: public informationin insects. Curr. Biol. 15,R869–R871.
4. Caro, T.M., and Hauser, M.D. (1992). Isthere teaching in nonhuman animals?Q. Rev. Biol. 67, 151–174.
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 74,128–148.
8. Franks, N.R., and Richardson, T. (2006).Teaching in tandem-running ants. Nature439, 153.
9. Holldobler, B., and Wilson, E.O. (1990).The Ants (Heidelberg Berlin: SpringerVerlag).
10. Dudai, Y. (1989). The Neurobiology ofMemory: Concepts, Findings, Trends(Oxford: Oxford University Press).
11. Tarpy, R.M. (1975). Basic Principles ofLearning (Glenview, Illinois: ScottForesman).
12. Giurfa, M., Zhang, S., Jenett, A., Menzel,R., and Srinivasan, M.V. (2001). Theconcepts of ‘sameness’ and ‘difference’ inan insect. Nature 410, 930–933.
13. Frisch, K.v. (1967). The Dance Languageand Orientation of Bees (Cambridge,Massachusetts: Harvard University Press).
14. Seeley, T.D. (1995). The Wisdom of theHive: The Social Physiology of Honey BeeColonies (Cambridge, Massachusetts:Harvard University Press).
School of Biological and ChemicalSciences, Queen Mary University ofLondon, Mile End Road, London E1 4NS,UK.E-mail: [email protected]
DOI: 10.1016/j.cub.2006.03.078
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