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carrying it, instead using a self-servingstrategy analogous to a rat on a sinkingship [3]. It can reduce its rate ofseparation from beneficial alleles bysuppressing recombination in fitindividuals, while escaping low-fitnessgenomesbypromoting recombination inthose. Little is known about the chemicalsignaling between A. nidulans coloniesthat leads to hyphal fusion, beyond theinvolvement of genes resembling thoseof theMAPkinasesignalingpathwaythatorchestratesmating inbuddingyeast [5],

but instigating fusion with neighbours,especially fitter ones, may be one wayfor a rat-like allele to switch vessels.

References1. Schoustra, S., Rundle, H., Dali, R., and

Kassen, R. (2010). Fitness-associated sexualreproduction in a filamentous fungus. Curr. Biol.20, 1350–1355.

2. Otto, S.P. (2009). The evolutionary enigma ofsex. Am. Nat. 174, S1–S14.

3. Hadany, L., and Otto, S.P. (2007). The evolutionof condition-dependent sex in the face of highcosts. Genetics 176, 1713–1727.

4. Dales, R.B.G., Moorehouse, J., and Croft, J.H.(1993). Evidence for a multi-allelic heterokaryon

incompatibility (het) locus detected byhybridization among threeheterokaryoncompatibility (h-c) groupsof Aspergillus nidulans. Heredity 70,537–543.

5. Glass, N.L., Rasmussen, C., Roca, M.G., andRead, N.D. (2004). Hyphal homing, fusion andmycelia interconnectedness. Trends Microbiol.12, 135–141.

Department of Biology, Wake ForestUniversity, P.O. Box 7325, Winston-Salem,NC 27109, USA.

DOI: 10.1016/j.cub.2010.06.008

Animal Cognition: Multi-modalInteractions in Ant Learning

A recent study shows that desert ants use a precise behaviour, based on theinternal cues of path integration, to facilitate the learning of visual landmarkinformation. This raises fascinating questions about how insects encodefamiliar terrain.

Paul Graham1, Andrew Philippides2

and Bart Baddeley2

Foraging ants must return to ofteninconspicuous nest entrances afterlong journeys using their two primarynavigational mechanisms, pathintegration and visual landmarkguidance. Path integration involvesthe continuous integration of directionand speed information to maintaina record of current position relativeto the start of a route [1]. In this way,ants can safely explore unfamiliarterrain whilst ‘connected’ to their nest.However, as it is based on internalcues, rather than external information,path integration is prone to cumulativeerror. To compensate for this, mostanimals also learn visual landmarksto specify important locations. Insectsuse visual information by storingtwo-dimensional retinotopic views,known as snapshots, of how theworld looked from goal locations [2–4].They can then return to a goal bycomparing their current view of theworld with the stored snapshot andusing the difference to determinea direction. It is widely held thatinsects, unlike mammals, do notcombine information derivedfrom these two mechanisms intoa ‘cognitive map’ [5]. However,observations of desert ants reportedin this issue by Muller and Wehner [6]

have reopened this debate bydemonstrating a role for precise pathintegration in the learning of visuallandmark information.

Visual landmark information is souseful that insects invest significanttime in ensuring it is accurate. Forexample, upon leaving an importantplace, wasps and bees performlearning flights, a series of arcs thatallow the bee or wasp to view the goalfrom directions that they will adopton subsequent return journeys [7–9].Analogous behaviours have also beenobserved in ants [10,11], althoughthese ‘learning walks’ have been lesswell-studied to date.

Muller and Wehner [6] have begun toprovide details of how learning walksare shaped to facilitate the learningof visual landmark information.The desert ant Ocymyrmex lives in afeatureless desert. Its path-integration-guided home runs often result ina prolonged search for aninconspicuous nest entrance(Supplemental data in [6]). Therefore,any information provided by locallandmarks is readily learnt. The authorsprompted a bout of learning byintroducing a prominent landmarkto the nest surroundings of anOcymyrmex nest. Upon noticing thechange, ants perform a neatlychoreographed learning walk beforedeparting on their foraging run.

The ants loop around the nest entrance,and at a series of points, they stopand rotate to accurately face the nest(Figure 1A). The brief periods whereants fixate the nest are an idealopportunity to store snapshots.One particularly interesting

characteristic of these learning walksis the accuracy with which ants face theinvisible nest entrance. This stronglysuggests the structure of these walksis tightly controlled by path integration.In fact, the authors hypothesise thatsnapshots stored when the ant isfacing the nest are labelled with thecurrent path integration co-ordinatesto generate a multi-modal spatialrepresentation which could be theprecursor to a ‘cognitive map’.However, this hypothesis is justone way that path integration andvision could interact and we considerother simpler possibilities. Futureexperiments addressing thesehypotheses are likely to provide insightinto the style and level of insectcognition.The simplest possibility is that ants

use path integration during the learningwalk only to ensure that a snapshotis learnt when the agent is directlyfacing the nest. This is sufficientfor subsequent homing becausesnapshots can be used as a visualcompass [12]. If panoramic images,from places near a goal, aresystematically rotated and eachrotation compared to a referencesnapshot taken at the goal, thenthe best match will be when theimage has a similar orientation tothat of the reference image.Figure 1B,C shows how with fourreference snapshots, centered onthe nest, one can derive nestwardsheadings from a large area. Here, path

B

Nest direction

i

ii

iv

iiiiii

iviii

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25 cm

Current Biology

Figure 1. Landmark learning in ant navigation.

(A) An example of a learning walk of the Namibian desert ant Ocymyrmex [6]. The ant leaves her nest (solid black square) after a black cylindricallandmark (solid black circle) has recently been placed nearby. (B) We simulate snapshot homing using panoramic images collected from groundlevel around an Australian desert ant nest. Four of the images (i–iv) are designated as snapshots, each of which is aligned to face the nest.(C) From the other locations, we derive headings for a hypothetical ant by using each snapshot as a visual compass. To recover a nestwardsorientation, we rotate images and find the orientation at which the rotated image best matches a snapshot. This process is performed indepen-dently for all four snapshots and the heading for our hypothetical ant is a weighted average (shown in vector plot) showing that ants could returnto the nest from any location.

Current Biology Vol 20 No 15R640

integration is used solely to orient theant during the learning of snapshotsand then discarded.

A next level of complexity would beto associate stored snapshots witha compass direction. With compassinformation, the current view of theworld can be aligned to the storedsnapshot. This is a prerequisite formost hypothetical models of snapshotuse. In such models, features commonto the current and stored snapshotsare identified and movement directionsare derived from the discrepancy intheir positions [13]. Wasps and beesalign themselves with stored viewsby translating whilst holding theirorientation fixed. Walking ants needa different solution to align the currentview with a stored snapshot.The required image rotation could beperformed neurally. Alternatively,ants could store a large set ofsnapshots at different orientations,something to which the learning walkis well-suited. Then, when returningto the nest, they would use the goalsnapshot which is closest in orientationto their current homeward path.

Muller and Wehner’s [6] hypothesisrepresents a third level of complexityin the way that path integration may becombined with view-based homing.Namely, labelling stored snapshotswith path integration co-ordinates.By identifying features or landmarksthat are common to differentsnapshots, one could use theco-ordinate information to builda map of the true metric positions

of those objects. Although notimpossible, this requires large amountsof computational power. A simplersolution would be to build a map inwhich whole snapshots are labelledwith their metric position derivedfrom path integration co-ordinates.Snapshots could then be usedto update or correct the currentco-ordinates of the path integrationsystem. This behaviour is seen inhamsters where brief viewing ofa familiar landmark array can resetthe path integrator [14]. Either of thesemap-like strategies would allow forcharacteristic behaviours such asthe aforementioned path integrationresetting and taking novel shortcuts.Behaviours, which it should bereiterated, have not yet been observedin ants [5,15].

Muller and Wehner [6] have shownbeautifully how path integrationand visual learning interact duringspecialized learning walks. We havediscussed mechanistic consequencesthat follow from this finding, includingthat path integration co-ordinatesneed not be tied to long-term visualmemories. Imminent researchaddressing these and otherhypotheses promises to give preciousinsight into the style and level of insectcognition.

References1. Muller, M., and Wehner, R. (1988). Path

integration in desert ants, Cataglyphis fortis.Proc. Nat. Acad. Sci. USA 85, 5287–5290.

2. Cartwright, B.A., and Collett, T.S. (1983).Landmark learning in bees. J. Comp. Physiol.151, 521–543.

3. Wehner, R., Michel, B., and Antonsen, P. (1996).Visual navigation in insects: coupling ofegocentric and geocentric information. J. Exp.Biol. 199, 141–146.

4. Durier, V., Graham, P., and Collett, T.S. (2003).Snapshot memories and landmark guidance inwood ants. Curr. Biol. 13, 1614–1618.

5. Collett, T.S., Graham, P., Harris, R.A., andHempel de Ibarra, N. (2006). Navigationalmemories in ants and bees: memory retrievalwhen selecting and following routes. Adv.Study Behav. 36, 123–172.

6. Muller, M., and Wehner, R. (2010). Pathintegration provides a scaffold for landmarklearning in desert ants. Curr. Biol. 20,1368–1371.

7. Van Iersel, J.J.A., and van den Assem, J. (1964).Aspects of orientation in the digger waspBembix rostrata. Anim. Behav. 1, 145–162.

8. Zeil, J. (1993). Orientation flights of solitarywasps (Cerceris; Sphecidae; Hymenoptera).J. Comp. Physiol. A. 172, 207–222.

9. Hempel de Ibarra, N., Philippides, A.,Riabinina, O., and Collett, T.S. (2009). Preferredviewing directions of bumblebees (Bombusterrestris L.) when learning and approachingtheir nest site. J. Exp. Biol. 212, 3193–3204.

10. Nicholson, D.J., Judd, S.P., Cartwright, B.A.,and Collett, T.S. (1999). Learning walks andlandmark guidance in wood ants (Formica rufa).J. Exp. Biol. 202, 1831–1838.

11. Wehner, R., Meier, C., and Zollikofer, C. (2004).Theontogenyof foragingbehaviour indesertants,Cataglyphis bicolor. Ecol. Entom. 29, 240–250.

12. Zeil, J., Hofmann, M., and Chahl, J.S. (2003).Catchment areas of panoramic snapshots inoutdoor scenes. J. Opt. Soc. Am. 20, 450–469.

13. Moller, R., and Vardy, A. (2006). Local visualhoming by matched-filter descent in imagedistances. Biol. Cyber. 95, 413–430.

14. Etienne, A.S., Maurer, R., Boulens, V., Levy, A.,and Rowe, T. (2004). Resetting the pathintegrator: a basic condition for route-basednavigation. J. Exp. Biol. 207, 1491–1508.

15. Wehner, R., Boyer, M., Loertscher, F.,Sommer, S., and Menzi, U. (2006). Antnavigation: one-way routes rather than maps.Curr. Biol. 16, 75–79.

1School of Life Sciences, UniversityofSussex,Brighton,UK. 2School of Informatics,University of Sussex, Brighton, UK.E-mail: p.r.graham@sussex.ac.uk

DOI: 10.1016/j.cub.2010.06.018