Integrative Cell Biology: Katanin at the Crossroads

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and regulation of the network, inparallel to its topology [9,19].

References1. Lin, D., Cao, L., Zhou, Z., Zhu, L., Ehrhardt, D.,

Yang, Z., and Fu, Y. (2013). Rho GTPasesignaling activates microtubule severing topromote microtubule ordering in Arabidopsis.Curr. Biol. 23, 290–297.

2. Fu, Y., Gu, Y., Zheng, Z., Wasteneys, G., andYang, Z. (2005). Arabidopsis interdigitating cellgrowth requires two antagonistic pathwayswith opposing action on cell morphogenesis.Cell 120, 687–700.

3. Fu, Y., Xu, T., Zhu, L., Wen, M., and Yang, Z.(2009). A ROP GTPase signaling pathwaycontrols cortical microtubule ordering and cellexpansion in Arabidopsis. Curr. Biol. 19,1827–1832.

4. Xu, T., Wen, M., Nagawa, S., Fu, Y., Chen, J.G.,Wu, M.J., Perrot-Rechenmann, C., Friml, J.,Jones, A.M., and Yang, Z. (2010). Cellsurface- and rho GTPase-based auxin signalingcontrols cellular interdigitation in Arabidopsis.Cell 143, 99–110.

5. Nagawa, S., Xu, T., Lin, D., Dhonukshe, P.,Zhang, X., Friml, J., Scheres, B., Fu, Y., andYang, Z. (2012). ROP GTPase-dependentactin microfilaments promote PIN1polarization by localized inhibition ofclathrin-dependent endocytosis. PLoS Biol.10, e1001299.

6. Roll-Mecak, A., and McNally, F.J. (2010).Microtubule-severing enzymes. Curr. Opin. CellBiol. 22, 96–103.

7. McNally, K., Audhya, A., Oegema, K., andMcNally, F.J. (2006).Katanincontrolsmitoticandmeiotic spindle length. J. Cell Biol. 175, 881–891.

8. Bichet, A., Desnos, T., Turner, S.,Grandjean, O., and Hofte, H. (2001). BOTERO1is required for normal orientation of corticalmicrotubules and anisotropic cell expansion inArabidopsis. Plant J. 25, 137–148.

9. Uyttewaal, M., Burian, A., Alim, K., Landrein, B.,Borowska-Wykret, D., Dedieu, A.,Peaucelle, A., Ludynia, M., Traas, J.,Boudaoud, A., et al. (2012). Mechanical stressacts via Katanin to amplify differences ingrowth rate between adjacent cells inArabidopsis. Cell 149, 439–451.

10. Bouquin, T., Mattsson, O., Naested, H.,Foster, R., and Mundy, J. (2003). TheArabidopsis lue1 mutant defines a katanin p60ortholog involved in hormonal control ofmicrotubule orientation during cell growth.J. Cell Sci. 116, 791–801.

11. Brodersen, P., Sakvarelidze-Achard, L.,Bruun-Rasmussen, M., Dunoyer, P.,Yamamoto, Y.Y., Sieburth, L., and Voinnet, O.(2008). Widespread translational inhibition byplant miRNAs and siRNAs. Science 320,1185–1190.

12. Stoppin-Mellet, V., Gaillard, J., and Vantard, M.(2006). Katanin’s severing activity favorsbundling of cortical microtubules in plants.Plant J. 46, 1009–1017.

13. Wasteneys, G.O., and Ambrose, J.C. (2009).Spatial organization of plant corticalmicrotubules: close encounters of the 2D kind.Trends Cell Biol. 19, 62–71.

14. Shaw, S.L., Kamyar, R., and Ehrhardt, D.W.(2003). Sustained microtubule treadmilling inArabidopsis cortical arrays. Science 300,1715–1718.

15. Eren, E.C., Dixit, R., and Gautam, N. (2010). Athree-dimensional computer simulation modelreveals the mechanisms for self-organization of

plant cortical microtubules into oblique arrays.Mol. Biol. Cell 21, 2674–2684.

16. Dhonukshe, P., Weits, D.A., Cruz-Ramirez, A.,Deinum, E.E., Tindemans, S.H., Kakar, K.,Prasad, K., Mahonen, A.P., Ambrose, C.,Sasabe, M., et al. (2012). A PLETHORA-auxintranscription module controls cell divisionplane rotation through MAP65 and CLASP. Cell149, 383–396.

17. La Rota, C., Chopard, J., Das, P.,Paindavoine, S., Rozier, F., Farcot, E.,Godin, C., Traas, J., and Moneger, F. (2011).A data-driven integrative model of sepalprimordium polarity in Arabidopsis. Plant Cell23, 4318–4333.

18. Ambrose, C., Allard, J.F., Cytrynbaum, E.N.,and Wasteneys, G.O. (2011). ACLASP-modulated cell edge barrier mechanismdrives cell-wide cortical microtubuleorganization in Arabidopsis. Nat. Commun.2, 430.

19. Locke, J.C., Young, J.W., Fontes, M.,Hernandez Jimenez, M.J., and Elowitz, M.B.(2011). Stochastic pulse regulation inbacterial stress response. Science 334,366–369.

1Laboratoire de Reproduction etDeveloppement des Plantes, INRA, CNRS,ENS, UCB Lyon 1, France. 2Laboratoire JoliotCurie, CNRS, ENS Lyon, Universite de Lyon,46 Allee d’Italie, 69364 Lyon Cedex 07,France.E-mail: Olivier.hamant@ens-lyon.fr

http://dx.doi.org/10.1016/j.cub.2013.01.031

Social Evolution: Policing withoutGenetic Conflict

Insect societies have evolved ways of policing selfish behaviour that arises dueto genetic conflicts within the colony. A new case of policing in an ant wherecolony members are genetically identical highlights the role of colonyeconomics for policing.

Benjamin P. Oldroyd

‘‘Conflict in insect societies isinevitable because insect societies arealmost always families not clones’’ [1].

Despite the many benefits, livingin a society has its drawbacks.Chief among these is the likelihoodthat some individuals willdisproportionately exploit the commonproperty of the society, to thedisadvantage of the majority. Takeparking. There’s nothing more irritatingthan someone parking you in. In factit’s so annoying that we (our society)pay people to walk around finingdouble parkers. In making andenforcing laws about parking, thecollective imposes its will over the

individual. This can be annoying whenwe personally get fined for what wasdefinitely a minor transgression thatdidn’t hurt anyone. In the end though,most of us grudgingly acknowledgethat without policing there would beparking anarchy and our parkingexperiences would be even lessconvivial. Thus, the inherent conflictbetween the individual and thecollective is managed by passinggenerally-agreed-to laws that areenforced by police. The principle ofpolicing can be scaled up to globalenforceable agreements, suchas those that may one day curbgreenhouse gas emissions, and downto insect societies, as emphasised ina new paper by Teseo and colleagues[2] in a recent issue of Current Biology.

There are at least four potentialconflicts that may afflict an insectsociety [1]: conflict over sex allocation(i.e. the proportion of male and femaleoffspring a colony should produce),conflict over caste fate (i.e. whichfemale larvae should develop asqueens — all would like to, but not allcan), conflict over queen production(workers might prefer their full sistersto become the daughter queens ofa colony rather than half sisters), andconflict over male production (shouldworkers or the queen be the mothersof the colony’s males?).These conflicts all arise from

asymmetries in relatedness betweenthe various members of a colony.Relatedness coefficients — theproportion of alleles in two individualsthat are identical by descent — arecomplicated to compute (interestedreaders may consult van Zweden et al.[3] for a pictorial summary), butconsider as an example the simplestcase of a haplo-diploid (queens arediploid, and haploid males producedby parthenogenesis) insect society inwhich there is a single queen thatmated once. In such cases, theworkers

Table 1. Examples of different uses of the word ‘policing’ in social insect research.

Kind of policing Basis Example Reference

Worker In polyandrous species workers are more related to

queen’s sons than the sons of other workers

Honey bees eat worker-laid eggs [6]

Classic Used to distinguish the kind of worker policing seen

in Apis from other forms of policing

[13]

Selfish Workers are more related to their own sons than

those of their sisters

Tree wasp workers eat the eggs of other workers [14]

Queen Queens are more related to their own sons than sons

of their daughters

Tree wasp queens eat worker-laid eggs [14]

Gamergate In queenless ants reproductive rate is determined by

position in the hierarchy of the reproductive workers

In Dinoponera quadriceps the dominant worker

chemically marks reproductive subordinates

that are then immobilized by other workers

[15]

Hygienic Workers may eat lower quality eggs laid by workers Honey bee workers, eggs have lower viability

than queen-laid eggs

[16] but see [13,17]

Self Workers refrain from activating their ovaries because

to do so is useless in the presence of coercive policing

In honey bees less than 1% of workers have

activated ovaries

[18]

Efficiency Inappropriate worker reproduction reduces colony

efficiency

In Cerapachys biroi workers attack reproductive

workers during periods when the colony is

non-reproductive

[2]

Figure 1. Cerapachys biroi worker tendinga larva.

The parthenogenetic ant Cerapachys biroiforms clonal societies that undergo stereo-typical reproductive cycles. Individuals thatdo not conform to these cycles are policedand executed, which is surprising given theabsence of genetic conflicts in this species.Photo by Serafino Teseo.

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are related to their own sons by ½, tothe sons of their sisters by 3/8 and tothe sons of the queen by ¼. The queenon the other hand is related to her sonsby ½. You can now see the potential forevolutionary conflict: the queens wouldprefer to monopolize the production ofmales, whereas workers would preferthat the queen stayed out of maleproduction and let them lay themale-producing eggs.

How do insect societies resolve theirinherent conflicts? Perhaps the bestunderstood example of conflictresolution concerns male production inthe honey bee, Apis mellifera. Honeybee queens are polyandrous, matingwith 10–20 haploid males [4]. Thismeans that a colony is composed ofa mixture of half sisters and full sisters.Francis Ratnieks [5] pointed out that onaverage a honey bee worker is relatedto the sons of the workers of her colonyby 1/8, whereas she is related to thesons of her queen by 1/4 and her ownsons by ½ (see the diagram in vanZweden et al. [3]). Again, this revealsthe potential for conflict betweenindividual workers (whichwould benefitfrom laying parthenogenetic eggs thatproduce sons) and the collectiveworkers (which prefer queen-laid eggsover worker-laid eggs).

How do the bees resolve thisconflict? Ratnieks [5] used populationgenetic modelling to show that allelesthat favour behaviour that decreasesthe proportion of worker-producedmales reared in favour of queen sonscan spread in a population. Suchbehaviour might include killing orharassment of reproductively-active

workers or selective removal ofworker-laid brood. Ratnieks coined anall-encompassing term for these kindsof behaviour ‘worker policing’ — themutual suppression of workerreproduction. In the following year,Ratnieks and Visscher [6] empiricallydemonstrated that honey bees haveindeed evolved policing behaviour.If you offer a honey bee colonyworker-laid eggs and queen-laid eggsthe worker-laid eggs are promptlyeaten, and the queen-laid ones areretained.

Honey bee worker egg-eating hasbecome the textbook example ofanimal policing [7]. The concept ofpolicing has broadened over the yearsfrom ‘worker policing’ to encompassother forms of policing (Table 1), but allexisting uses of the term ‘policing’ havetheir antecedents in the conflictsarising from asymmetrical relatedness.However, Teseo et al. [2] have nowdemonstrated a new class of policingbehaviour in the brood-raiding Asianant Cerapachys biroi (Figure 1). As thisspecies is obligately clonal, its coloniesare entirely free of conflicts arisingfrom genetic asymmetries. Yet, theseants kill sister workers that try toreproduce. Why?

In Ratnieks’ [5] original casting of thetheory of worker policing he noted thatif worker reproduction reduced colonyefficiency, then this could enhance theevolution of policing behaviour. InC. biroi, as Teseo et al. [2] demonstrate,policing appears to function solely asan enhancer of colony efficiency.C. biroi has an unusual reproductivecycle that consists of alternating

reproductive and foraging phases [8].During the reproductive phase (about3 weeks) many of the workers laydiploid eggs. Then, as the larvaeappear, the workers stop laying eggsand concentrate on stealing the eggs ofother species to feed the larvae. Theforaging phase lasts a bit over twoweeks. During the foraging phase,most workers respond to the presenceof larvae in their nest, and refrain fromreproducing. Teseo et al. [2] show thatduring this foraging phase workers thatfail to respond to the larval signals arekilled by the other workers. Thus, theants are policing their recalcitrantsisters, not because they are in

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competition over who shall reproduce,but because it is apparently moreefficient for the colony to cyclebetween phases of reproduction andforaging. Why cycling should bemore efficient than continuousreproduction, as is seen in mosteusocial insects, has not yet beenaddressed. Perhaps it is the only waythese ants can control egg production.Interestingly, females of some solitaryinsects show similar cycling, and someaspects of the behaviour of eusocialspecies may be derived from thesecycles [9].

The Teseo paper [2] is importantbecause it brings into sharp focus therelative importance of colony conflictand colony efficiency in the evolution ofworker policing. In all other studysystems, conflict and efficiency areconfounded. A honey bee colony isless efficient if the workers lay eggs[10,11], but did policing first evolve toreduce genetic conflict or increasecolony-level efficiency? Teseo et al. [2]have demonstrated that efficiencyalone seems to maintain policing inC. biroi, but it still seems that in mostother cases it is kin conflict that hasdriven the evolution of worker policing.Predictions about policing behaviourfrom conflict theory are stronglysupported empirically [1,12]. So, itseems that both conflict and efficiencycan be important to the evolution ofpolicing. It is interesting to speculateon whether the policing behaviour

observed in C. biroi originally evolvedto resolve genetic conflict, and wasthen co-opted to its present function,or if it arose when the species becameclonal, abandoned queens andadopted its current practise ofreproductive cycling. In any case, itis now timely to re-emphasise thatthe concept of worker policingencompasses behaviour that improvescolony efficiency as well as resolvingconflict [13].

References1. Ratnieks, F.L.W., Foster, K.R., and

Wenseleers, T. (2006). Conflict resolution ininsect societies. Annu. Rev. Ent. 51,581–608.

2. Teseo, S., Kronauer, D.J.C., Jaisson, P., andChaline, N. (2013). Enforcement of reproductivesynchrony via policing in a clonal ant. Curr.Biol. 23, 328–332.

3. van Zweden, J.S., Cardoen, D., andWenseleers, T. (2012). Social evolution: Whenpromiscuity breeds cooperation. Curr. Biol. 22,R922.

4. Palmer, K.A., and Oldroyd, B.P. (2000).Evolution of multiple mating in the genus Apis.Apidologie 31, 235–248.

5. Ratnieks, F.L.W. (1988). Reproductiveharmony via mutual policing by workersin eusocial. Hymenoptera. Am. Nat. 132,217–236.

6. Ratnieks, F.L.W., and Visscher, P.K. (1989).Worker policing in honeybees. Nature 342,796–797.

7. Davies, N.B., Krebs, C.J., and West, S.A. (2012).An Introduction to Behavioural Ecology, 4thEdition (Chichester: Wiley-Blackwell).

8. Ravary, F., and Jaisson, P. (2002). Thereproductive cycle of thelytokous colonies ofCerapachys biroi Forel (Formicidae,Cerapachyinae). Ins. Soc. 49, 114–119.

9. Amdam, G.V., Csondes, A., Fondrk, M.K., andPage, R.E. (2006). Complex social behaviourderived from maternal reproductive traits.Nature 439, 76–78.

10. Montague, C.E., and Oldroyd, B.P. (1998). Theevolution of worker sterility in honey bees: aninvestigation into a behavioral mutant causinga failure of worker policing. Evolution 52,1408–1415.

11. Barron, A.B., Oldroyd, B.P., andRatnieks, F.L.W. (2001). Worker reproductionin honey-bees (Apis) and the anarchicsyndrome: A review. Behav. Ecol. Sociobiol.50, 199–208.

12. Wenseleers, T., Badcock, N.S., Erven, K.,Tofilski, A., Nascimento, F.S., Hart, A.G.,Burke, T.A., Archer, M.E., and Ratnieks, F.L.W.(2005). A test of worker policing theory in anadvanced eusocial wasp, Vespula rufa.Evolution 59, 1306–1314.

13. Zanette, L.R.S., Miller, S.D.L., Faria, C.M.A.,Almond, E.J., Huggins, T.J., Jordan, W.C., andBourke, A.F.G. (2012). Reproductive conflict inbumblebees and the evolution of workerpolicing. Evolution 66, 3765–3777.

14. Wenseleers, T., Tofilski, A., andRatnieks, F.L.W. (2005). Queen and workerpolicing in the tree wasp Dolichovespulasylvestris. Behav. Ecol. Sociobiol. 58,80–86.

15. Monnin, T., Ratnieks, F.L.W., Jones, G.R., andBeard, R. (2002). Pretender punishmentinduced by chemical signalling in a queenlessant. Nature 419, 61–65.

16. Pirk, C.W.W., Neumann, P., Hepburn, H.R.,Moritz, R.F.A., and Tautz, J. (2004). Egg viabilityand worker policing in honey bees. Proc. Nat.Acad. Sci. USA 101, 8649–8651.

17. Beekman, M., and Oldroyd, B.P. (2005). Honeybee workers use cues other than egg viabilityfor policing. Biol. Lett. 1, 129–132.

18. Wenseleers, T., Hart, A.G., and Ratnieks, F.L.W.(2004). When resistance is useless: Policingand the evolution of reproductive acquiescencein insect societies. Am. Nat. 164,E154–E167.

Behaviour and Genetics of Social InsectsLab, School of Biological Sciences A12,University of Sydney, Sydney, NSW 2006,Australia.E-mail: benjamin.oldroyd@sydney.edu.au

http://dx.doi.org/10.1016/j.cub.2013.01.051

Cognitive Neuroscience: TargetingNeuroplasticity with Neural Decodingand Biofeedback

New research combining neural decoding and biofeedback to targetneuroplasticity causally links early visual cortical plasticity with improvedperception. This is an exciting new approach to understanding brain function,one which may lead to new ways of treating neurological disorders by targetedintervention.

Aaron R. Seitz

A central goal of cognitiveneuroscience is to understand howbrains give rise to behavior. The holygrail of many fields of cognitiveneuroscience is to make causal linksbetween the processing within, or

between, various brain regions andpeople’s perceptions, decisions oractions. Establishing such causalitybetween brain and behavior isextremely difficult given that so manybrain regions are normally active duringtask performance, that correlationsbetween brain processing and

behavior can be spurious orepiphenomenal, and that thedirectionality of such correlations isalways ambiguous. Here we discusstwo new studies [1,2] that haveovercome these limitations by usinga novel approach combining neuraldecoding of functional magneticresonance imaging (fMRI) signals withbiofeedback to target neuroplasticitywithin specific brain regions.In the field of perceptual learning,

there has been a long and heateddebate regarding the role of early visualcortical plasticity in perceptual learning[3]. To date, the case for early visualcortex being important in behaviorallearning effects has been based uponcorrelational arguments, and whilethere are numerous demonstrations ofplasticity as early as primary visual