efficient kinetochore capture. J. Cell Biol.173, 879–891.

8. Howard, M., and Kruse, K. (2005).Cellular organization byself-organization: mechanismsand models for Min proteindynamics. J. Cell Biol. 168,533–536.

9. Thanbichler, M., and Shapiro, L. (2006).MipZ, a spatial regulator coordinatingchromosome segregation with celldivision in Caulobacter. Cell 126, 147–162.

10. Elowitz, M.B., Levine, A.J., Siggia, E.D.,and Swain, P.S. (2002). Stochastic geneexpression in a single cell. Science 297,1183–1186.

Department of Mathematics, ImperialCollege London, South KensingtonCampus, London SW7 2AZ, UK.E-mail: mjhowa@imperial.ac.uk

DOI: 10.1016/j.cub.2006.08.014

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Parenting Behaviour: BabblingBird Teachers?

One of humankind’s most distinctive characteristics is our extended andcomplex period of child dependency. New research on a noisy African birdmay help to shed light on how our unusual parenting behavior evolved.

Lisa G. Rapaport

We humans are extraordinarilysolicitous parents. This is not to saythat intensive infant-care duties,like feeding and keeping watchover baby, are so remarkable.Other primates do the same fortheir infants, and many othervertebrate species do, too. Whatmakes us stand out as parents areboth the duration (relative tolifespan) and complexity of ourcaretaking behavior. New researchfrom an unexpected source,reported in this issue of CurrentBiology [1], may help to shed lighton how our unusual parentingbehavior evolved.

Unlike most other animals,human parents continue to investin their offspring well intoadulthood. For example, in ruralEthiopia, mothers regularly visittheir married daughters’households, helping with heavydomestic chores, and in so doingincrease the survival prospects oftheir grandchildren [2]. Inindustrialized nations, parentsoften invest extensively in theirchildren’s education to help themsucceed in a competitiveenvironment. Many of the readersof this article undoubtedly knowfamilies who have even welcomedback into the parental nestoffspring who have finishedcollege but just have not yet beenable to land that lucrative job.

Human parental care is complexbecause it is characterized bychanges in the type of care offeredas the child matures; emphasisshifts during development from

providing for nutritional and otherbasic physical needs to trainingand encouragement. This lengthyperiod of dependency is integral towho we are as a species.Anthropologists have argued thatin subsidizing the diets of younggroup members, provisioningsupported a prolonged learningperiod, and was the lynchpin thatpermitted our ancestors tospecialize on increasingly variedand difficult-to-acquire resources,and the technological advancesused to exploit them [3].

Given such importance to thehuman life history strategy, onemight expect to find an extendedperiod of provisioning as well asadult instruction orencouragement of offspringlearning among our primaterelatives, at least in nascent form.But provisioning of weaned younggenerally is infrequent and activesupport of skill development isvirtually nonexistent. Whena human child takes on a new skill,his or her caregiver often plays afacilitating role. Among nonhumanprimates, in contrast, learningis a much more exclusivelyself-motivated proposition [4]. Ayoung wild chimpanzee mustlearn to recognize and processhundreds of different kinds of foodby paying close attention to whatthe mother and other adults eat.A mother usually tolerates herjuvenile feeding in the same areaand taking an occasional scrap offood, but even complex foragingtechniques such as termite-fishing(in which a tool, designed fromnearby vegetation, is inserted into

a mound to extract termites) andother types of tool use are learnedwithout active guidance fromadults [5,6].

In this issue, Radford and Ridley[1] report how wild adult piedbabblers modify their caretakingbehavior in a way that may favorlearning by juveniles. Piedbabblers (Turdoides bicolor) aremedium-sized passerine birds ofsouthern Africa, noted for theirsteady chattering contactcalls — hence the name. Theyinhabit scrubby acacia woodlandsand savanna, and spend much oftheir time foraging on the groundfor invertebrates [7]. Groupstypically consist of one breedingpair and several non-reproductiveadults, all of whom help to care forthe group’s altricial young, a typeof social system calledcooperative breeding [8,9]. Thestudy’s most remarkableobservation is not that piedbabblers provision their group’syoung: all birds who have helpless,relatively immobile hatchlingsmust provision their young. Nor isit that adults preferentially allowfledglings to share their foragingsites with them: tolerance forimmatures while foraging is knownin a variety of bird species [10–12].The striking finding is that adultsappear to take an active andvariable role in the development oftheir fledglings’ foraging abilities.

Radford and Ridley [1] observedthat, a few days before young piedbabblers fledge, adults begin toemit a soft ‘purr’ vocalization whenthey bring food to the nest. Uponfledging, the young follow foragingadults and solicit food from them(Figure 1), while adults, for theirpart, continue to use the purrvocalization during provisioninginteractions. It is at this point thatadults begin to purr-call from timeto time in a new context: whileforaging. Using playbacks of calls,experiments with supplemental

Current Biology Vol 16 No 17R676

Figure 1. An adult pied babbler, with well-defined black and white coloration, offersfood to a conspicuously begging fledgling. (Photo by A.N. Radford.)

food, and observations ofunmanipulated behavior, theauthors found that adultspurr-called most frequently whenthe group contained fledglings,that fledglings approached inresponse to calls more often thanadults (and when adults didapproach, they were often chasedaway by the caller), and that foodpatches were depleted morerapidly when a fledgling joined thecaller to feed.

The babblers’ age-sensitivecaretaking behavior meets threeof the four objective criteriaproposed by Caro and Hauser [13]to qualify as teaching: the adultsmodify their behavior in thepresence of inexperiencedindividuals; calling is costly toadults in terms of time spentfeeding in a patch; and byrecruiting fledglings to productiveforaging patches, the adults’behavior encourages them to gainage-appropriate experience.Because Radford and Ridley [1] donot specifically address the issueof teaching, they did not attemptto determine whether babblersmeet the remaining criterion, thatinexperienced individuals acquireinformation or skill more quickly asa result of such guidance.Nonetheless, the babbler’srecruitment calling may evenqualify as teaching under a morestringent definition: that theinformation transferred facilitateslearning of skills and strategies,

rather than simple facts such asthe locations of foraging sites [14].With the exception of termitenests, which are relativelypermanent fixtures in thelandscape, babbler foragingpatches are ephemeral and so anyinformation value to fledglingsmay have more to do with whata good foraging patch should looklike rather than a specific foragingsite’s location.

Radford and Ridley’s articlefollows on the heels of a report onteaching in meerkats [15]. Thesecooperatively breeding Africanmongooses encourage their pupsto develop prey-handling skills,particularly with regard todangerous prey like scorpions. Asthe pups grow, adults increasinglyrefrain from killing the prey theygive to them and with suchexperience pups learn effectiveprey-dispatch methods, thussatisfying Caro and Hauser’s [13]fourth criterion. The meerkatresults [15] are consistent withprevious, largely anecdotalevidence suggesting that routineteaching is most pervasive amongpredators, such as raptors, felids,and orcas, that train their young tohunt [13,16]. It has been widelyaccepted that the selective forcefavoring active parental guidanceof skill development is a dietaryniche, like reliance on large prey,that is both challenging andhazardous. Radford and Ridley’s[1] research calls this supposition

into question. Pied babblers dooccasionally eat scorpions, lizardsand small snakes, but adults tendto recruit fledglings to feed oninnocuous insects [1,7].

The question is whether riskyforaging strategies or some otheraspect of the babblers’ biologyhas favored their unusualsequence of caretaking behavior.One clue brings us back to theprimates. The only other species inwhich recruitment calling tojuveniles has been documented,besides felids, is a diminutiveSouth American monkey, thegolden lion tamarin [17,18]. In themonkeys’ case, the callsencourage juveniles to search forhidden prey. Like pied babblersand meerkats, tamarins provisiontheir young — and are cooperativebreeders. Historically, we humans,too, have been cooperativebreeders, in that mothers haveconsistently relied on relatives forchildcare assistance [2,19]. Couldit be that sharing responsibilitiesamong multiple group memberssomehow favors prolonged andcomplex caretaking behavior, andeven teaching? If so, we may havea lot to learn from other animalsthat cooperate to care for theiryoung. Radford and Ridley’s [1]research should stimulate awide-ranging search for answers.

References1. Radford, A.N., and Ridley, A.R. (2006).

Recruitment calling: a novel form ofextended parental care in an altricialspecies. Curr. Biol. 16, 1700–1704.

2. Gibson, M.A., and Mace, R. (2005).Helpful grandmothers in rural Ethiopia:a study of the effect of kin on childsurvival and growth. Evol. Hum. Behav.36, 469–482.

3. Kaplan, H., Hill, K., Lancaster, J., andHurtado, A.M. (2000). A theory of humanlife history evolution: diet, intelligence,and longevity. Evol. Anthropol. 9,156–185.

4. King, B.J. (1994). Primate infants asskilled information gatherers. Pre-Perinatal Psychol. J. 8, 287–307.

5. Lonsdorf, E.V. (2006). What is the role ofmothers in the acquisition of termite-fishing behaviors in wild chimpanzees(Pan troglodytes schweinfurthii)? Anim.Cong. 9, 36–46.

6. Matsuzawa, T., Biro, D., Humle, T.,Inoue-Nakamura, N., Tonooka, R., andYamakosi, G. (2001). Emergence ofculture in wild chimpanzees: educationby master-apprenticeship. In PrimateOrigins of Human Cognition andBehavior, T. Matsuzawa, ed. (TokyoBerlin Heidelberg: Springer),pp. 557–574.

7. Ridley, A. (n.d.). Pied Babbler ResearchProject. Retrieved June 29, 2006, from:http://www.zoo.cam.ac.uk/zoostaff/larg/pages/home.html.

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8. Emlen, S.T. (1984). Cooperative breedingin birds and mammals. In BehavioralEcology: An Evolutionary Approach,J.R. Krebs and N.B. Davies, eds.(Sunderland, MS: Sinauer), pp. 305–339.

9. W.D. Koenig and D.L. Dickinson, eds.(2004). Ecology and Evolution ofCooperative Breeding in Birds(Cambridge: Cambridge UniversityPress).

10. Diamond, J., and Bond, A.B. (1991).Social behavior and the ontogeny offoraging in the kea (Nestor notabilis).Ethology 88, 128–144.

11. Langen, T.A. (1996). Skill acquisition andthe timing of natal dispersal in the white-throated magpie-jay, Calocitta formosa.Anim. Behav. 51, 575–588.

12. Sullivan, K.A. (1988). Ontogeny of timebudgets in yellow-eyed juncos:adaptation to ecological constraints.Ecology 69, 118–124.

Chromosome SegCorrecting ImpropChromosomes

Two new studies show that Aurora Battached chromosomes by recruitingeliminating the bad attachments andkinetochore fiber.

Xin Zhang and Claire E. Walczak

The proper segregation ofchromosomes to the two daughtercells is an essential part of the cellcycle. Defects in this processresult in aneuploidy, which canlead to genomic instability andcancer. Accurate chromosomesegregation in mitosis requiresthat sister kinetochores on themitotic chromosomes attachproperly to microtubulesemanating from opposite spindlepoles, but the molecularmechanisms underlying thisprocess are not yet understood.One key player in sensing andcorrecting improperkinetochore–microtubuleattachments is Aurora B kinase,inhibition of which results inmultiple mitotic defects, includingthe failure to detect or correctimproper attachments.Understanding how Aurora Bworks requires the identification ofkey downstream substrates, suchas the microtubule depolymerizingkinesin, MCAK, which is alsoinvolved in regulating properkinetochore–microtubuleinteractions. Two papers in this

13. Caro, T.M., and Hauser, M.D. (1992).Is there teaching in nonhumananimals? Quart. Rev. Biol. 67,151–172.

14. Leadbeater, E., Raine, N.E., and Chittka, L.(2006). Social learning: ants and themeaning of teaching. Curr. Biol. 16,R323–R325.

15. Thornton, A., and McAuliffe, K. (2006).Teaching in wild meerkats. Science 313,227–229.

16. Boran, J.R., and Heimlich, S.L. (1999).Social learning in cetaceans: hunting,hearing and hierarchies. In MammalianSocial Learning: Comparative andEcological Perspectives, H.O. Box andK.R. Gibson, eds. (Cambridge:Cambridge University Press),pp. 282–307.

17. Rapaport, L.G., and Ruiz-Miranda, C.R.(2002). Tutoring in wild golden lion

regation:erly Attached

kinase corrects improperlymolecules necessary forby regulating the turnover of the

issue [1,2] reveal some new hintsabout the mechanism by whichAurora B corrects improperattachments. These studies showthat molecules such as MCAK andthe Aurora B complex itself areselectively and preferentiallylocalized to defective attachmentsites, where they act to control theattachment state by regulatingthe dynamics of thekinetochore-fibers.

In vertebrate cells, thekinetochores are attached to thespindle poles by bundles ofmicrotubules that form thekinetochore-fibers. Defectiveattachments, such as merotelicattachments in which a singlekinetochore is attached tomicrotubules emanating from bothspindle poles, are particularlydamaging because they are notsensed by the spindle assemblycheckpoint, but do cause laggingchromosomes during mitosis[3,4]. Luckily for cells, merotelicattachments occur frequently inearly mitosis, but most arecorrected before anaphase by asyet unknown mechanisms [5]. Ithas recently been shown thatmany of the merotelic attachments

tamarins. Int. J. Primatol. 23,1063–1070.

18. Rapaport, L.G. (2006). Provisioning inwild golden lion tamarins: benefits toomnivorous young. Behav. Ecol. 17,212–221.

19. Hrdy, B.S. (2005). Comes the child beforeman. In Hunter-Gatherer Childhoods:Evolutionary, Developmental andCultural Perspectives, B.S. Hewlett andM.E. Lamb, eds. (New Brunswick: AldineTransaction), pp. 65–91.

Clemson University, Department ofBiological Sciences, 132 Long Hall,Clemson, South Carolina 29634, USA.E-mail: lrapapo@clemson.edu

DOI: 10.1016/j.cub.2006.08.012

that persist in anaphase often getsegregated to the pole with thethicker kinetochore-fiber bundle,which is presumably the correctspindle pole. But then how doesAurora B function in this process?

Cimini et al. [1] took advantageof a small molecule inhibitor ofAurora B, ZM44739 [6], to partiallyinhibit Aurora kinase and thenexamined the properties of thekinetochore-fibers. They foundthat partial inhibition of Aurora Bkinase resulted in an accumulationof lagging chromosomes atanaphase, in part by increasing thefraction of microtubules that areattached to the incorrect pole.To look more closely at themicrotubules within thekinetochore-fiber, they useda photoactivatable derivative ofthe fluorescent fusion proteinGFP-tubulin to measure thedynamics of the microtubuleswithin the kinetochore-fiber. Theyfound that partial inhibition ofAurora B caused a dramaticstabilization of thekinetochore-fibers, but had noeffect on the turnover of bulkspindle microtubules. Thisprovides a potential explanationfor why the attachments are notcorrected, because themicrotubules within thekinetochore-fiber are unlikely to bedetaching from the kinetochore.

Interestingly, while the dynamicsof the kinetochore-fibermicrotubules were dramaticallyreduced by Aurora B inhibition, theamount of tension between thetwo sister kinetochores was notsignificantly perturbed. This