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Navigation: from animal behaviour to guiding principles

Whether an animal’s world is restricted to afew twigs or the avian highways thattraverse the planet, creatures must navigatetheir surroundings with every fin stroke,wing beat and stride. ‘Navigation is one ofthe basic problems that almost all mobileanimals, including ourselves, have tosolve’, says JEB Editor Almut Kelber fromthe University of Lund, Sweden. Humanshave been fascinated by animals’navigational abilities for centuries. Inrecent years, scientists have begununravelling the mysteries of navigation ongrand and small scales, to reveal themechanisms that allow some to determinetheir direction of travel, the distances thatthey must cover and the sensory systemsthat guide them. However, Kelber explainsthat the concepts and techniques used bythe communities that study animalnavigation in organisms from insects tomammals vary significantly, and there islittle discussion between these groups.Excited by the prospects offered byrecently developed techniques, which willallow scientists to identify the essentialgenes and neural circuits that controlnavigation, Kelber has compileda collection of inspirational Reviewarticles,which discuss navigational behaviours,

sensory guidance systems and themechanisms that allow animals to maintaina sense of location and set a bearing.

Animals and their maps‘I wanted to bring together work thatreally describes animal behaviour indetail’, says Kelber, who invited RussellWyeth from St Francis Xavier University,Canada, to review what is currentlyknown about navigation in aquaticgastropods ( jeb185843). Guided bya wide range of senses, the slowly movingcreatures frequently pursue odours insearch of food and mates, in addition tofleeing the scent of predators. Explaininghow the molluscs might follow attractiveodours – either by moving in the directionof the water flow carrying the odour, or bymoving toward the position where theodour is strongest – Wyeth outlinesthe circuitry that guides gastropods;from the sensory neurons that detectscents to the motor neurons that drive theirmovements and the control circuits thatdetermine when the animals turn.

While a keen sense of smell is essentialfor gastropods in search of food, GabrieleGerlach from the University of

Oldenburg, Germany, and colleaguesdescribe how larval reef fish also followtheir sense of smell when returning home,after having been washed out to sea( jeb189746). As it currently is notpossible to investigate the neuralmechanisms that allow reef fish tonavigate home, the team has switchedfocus to the better-understood zebrafish.They discovered that 6-day-old zebrafishlarvae must be able to see each other tolearn to associate the scent of the waterwith their siblings, the presence of whichindicates that they are ‘home’. It seemsthat the larvae also learn to sniff out aspecific class of proteins produced by theimmune system – majorhistocompatibility complex proteins – toidentify related fish that also define home.Gerlach then outlines evidencesupporting the possibility that crypt cells,a type of nerve cell that contributes toscent recognition in other species, may beinvolved in zebrafish and reef fishhoming.

However, the scale of the challenge facedby returning reef fish pales intoinsignificance alongside the ocean-wideodysseys upon which sea turtles andsalmon embark. Kenneth and CatherineLohmann from the University of NorthCarolina, USA, explain that adult turtlesand salmon navigate back to their area of

Tritonia diomedea navigating through a sea pen bed in search of prey or mates.Photo credit: Russell Wyeth and James A. Murray.

Loggerhead sea turtle (Caretta caretta)hatchlings. Photo credit: Kenneth Lohmann.

Inside JEB highlights the key developments in Journal of Experimental Biology.Written by science journalists, each short report gives the inside view ofthe science in JEB.

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© 2019. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2019) 222, jeb199752. doi:10.1242/jeb.199752

origin predominantly using a magneticsense, adjusting their bearings as theyvoyage across oceans by detecting subtledifferences in the geomagnetic field( jeb184077). While salmon resort tofollowing their sense of smell during thefinal approach to their spawning grounds,female turtles locate their home beachesby seeking out the magnetic signature thatdistinguishes their nesting beach fromothers.

Moving on from the challenge of long-distance aquatic navigation, BarbaraWebb from the University of Edinburgh,UK, reviews some of the impressivebreakthroughs that have been maderecently in our understanding of thenavigation mechanisms used by insectssuch as ants and bees ( jeb188094). Webbdescribes developing a powerfulmathematical model that accuratelyreproduces the insects’ navigationalpowers based on three factors: their abilityto return home directly after following acircuitous outbound path (known as pathintegration); their ability to memorize theposition of significant locations, such asfood sites, and subsequently use thememory to return to those locations; anda visual memory of the surrounding area,which the insect matches with its currentview, to maintain its course. Althoughshe warns that this model does notexplain all aspects of the insects’extraordinary navigational abilities,Webb has used the insect-inspiredstrategy to design successful robotguidance systems.

While ants and bees cover great distancesduring daily foraging excursions, theirventures are on a far smaller scale than theannual migrations undertaken by someinsects and birds. Focusing on theEuropean blackcap and North Americanmonarch butterfly populations, both ofwhich perform migrations over hundredsand thousands of kilometres, ChristineMerlin from Texas A&M University,USA, and Miriam Liedvogel from theMax Planck Institute for EvolutionaryBiology, Germany, explain that we arebeginning to learn more about thegenetics of long-distance navigation( jeb191890). They review how asignificant proportion of the differences inthe migratory strategies used by distinctblackcap populations can be attributed totheir genetic differences, while theexpression of specific genes, which areepigenetically regulated, accounts for the

monarch butterflies’ intergenerationalmigration. They add that the use of novelgenetic techniques is revolutionising ourunderstanding of navigation and willallow researchers to identify key genesand regulatory pathways modulating theseextraordinary odysseys.

Considering the mechanism that humansuse to negotiate their environment,William Warren from Brown University,USA, blows apart the conventional myththat humans navigate according to atraditional map carried in the head( jeb187971). Describing experimentsbased on a virtual reality maze linkingeight locations that participants couldexplore, Warren explains that the mazeincluded an impossible twist – two‘wormholes’ between remote positions inthe maze – allowing him to essentiallyteleport volunteers to a new location androtate them by 90 deg. Surprisingly, theparticipants were completely unaware ofthe relocation, yet when asked to takeshortcuts in a subsequent test, theyexploited the wormholes. Based on thisbehaviour, Warren suggests that weperceive the world as a ‘network of pathsbetween places that are augmented withlocal metric information’, and he explainsthat his strategy allows us to find newroutes to familiar locations, makesuccessful detours, and even take roughshortcuts.

Technical developmentsAlthough many species depend on a rangeof familiar senses for navigation, othercreatures depend on senses that arecompletely alien to us. Emerging fromtheir roosts after dark, bats use ultrasoundcries for high-precision navigation,hunting and communication. Yossi Yoveland Stefan Greif from Tel AvivUniversity, Israel, review how recentdevelopments in miniature tag design

now make it possible for researchers toeavesdrop directly on the echolocationcalls of bats while simultaneouslyrecording their behaviour ( jeb184689).They outline what we can learn about thenavigation strategies of other animals,their diets and how they forage, as well associal interactions and communicationusing on-board technology. In addition,they suggest that tagged animals couldspy on other species, allowing researchersto learn about animals that wouldotherwise be impossible to investigate,exploiting acoustic information to gleaninformation about their movements, theenvironment that they are moving throughand even their breath rate.

In another technological breakthrough,Nadine Diersch and Thomas Wolbers,from the German Centre forNeurodegenerative Diseases, review howvirtual reality is helping us to understandthe loss of spatial awareness thataccompanies neurodegenerative diseaseand ageing in humans and rodents( jeb187252). They say that virtual realitysimulations allow researchers to createrealistic environments while tracking themovements and reactions of volunteersmoving through situations that would beimpossible in the real world. However,they warn that there are drawbacks to theuse of virtual reality when working withthe elderly. These include the lack ofadditional physical cues – such asinformation about the position of anindividual’s body in space – which mayalter the participant’s perceptions andbehaviour, as well as the increased riskof cyber sickness in older people, whoare often less familiar with virtual realitytechnology.

Neural control of navigationShifting focus from navigationalbehaviour to the neural systems thatintegrate sensory information to guidenavigation, Kelber says, ‘Animals are not

A simulation of a personwalking through a virtualreality maze. Photo credit: William Warren.

Tagged Egyptian fruit bats (Rousettusaegyptiacus). Photo credit: Michal Samuni.

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machines, so their navigationmechanisms are not designed byengineers, but have been evolved overmillions of years in a changing world.I find it highly fascinating how suchsystems function’.

Introducing us to the central complex, theregion of the brain that controlsnavigational behaviour in insects, StanleyHeinze and colleagues from LundUniversity, Sweden, explain that thestructure has remained virtuallyunchanged for 400 million years.Collating sensory inputs from theantennae, wings and visual system, thecentral complex integrates this withinformation about the position of objectsin the sky, such as the sun or moon –which are distant and can function as acompass – allowing animals to take abearing ( jeb188854). Heinze adds thatthe ability to set and maintain anavigational bearing is essential for awide range of navigational applications,including long-range navigation, homingand following a perfectly straight line.

Although fruit flies (Drosophilamelanogaster) do not have a reputationfor migrating, Timothy Warren, YsabelGiraldo and Michael Dickinson from TheCalifornia Institute of Technology, USA,suggest that the ubiquitous insects owetheir global distribution to an ability tomigrate ( jeb186148). The flies depend ontheir knowledge of the position of the sunor moon – gleaned through directobservation, by orientation relative to thepattern of polarized light in the sky, orfrom the light intensity gradient in thesky – to determine a fixed bearing.Drawing parallels between the structure ofthe fly central complex and that of thelong-distance migratory locust, Warrenand colleagues suggest that

D. melanogaster select their bearing earlyin flight, rather than aiming for agenetically preselected goal. They alsoadd that the wealth of molecular toolsavailable to study the minute insects couldallow researchers to study the neuralcircuitry underlying navigation in waysthat would be impossible in other species.

Dung beetles are also not renowned forlong-range navigational feats, but Basil elJundi and a team of internationalcollaborators describe how the insects areable to perform a simpler navigationalfeat. They roll dung balls in reverse alongperfectly straight lines and can evenresume their linear path after deviatingaround bushes and other obstacles. elJundi explains that the beetles collect avisual snapshot of the sky prior to settingout and process information about theposition of the sun, moon or the pattern ofpolarized light in the sky in the centralcomplex before setting the straightbearing that they follow ( jeb192450).Comparing the structure of the dungbeetle’s central complex with that ofinsects that navigate over greaterdistances, the collaborators admit thatthey are surprised by the structuralsimilarities despite the vastly differentscales of the navigational challenges.

In contrast to the Reviews discussinginsect navigation, Francesco Savelli andJames Knierim, from Johns HopkinsUniversity, USA, discuss the role of oneof the main regions that allows mammalsto keep track of their location, thehippocampal formation, which useslandmarks and the sensations generatedby the individual’s movements togenerate a sense of position ( jeb188912).Describing how one class ofhippocampus cells, known as ‘placecells’, record the position of an individualin their internal spatial map, the duodiscuss ‘grid cells’ – a class of nerve cellthat possibly keeps track of an

individual’s motion through pathintegration to generate a sense of position.They go on to review robotic algorithmsas well as computer simulations based onthe interplay between hippocampal spatialcells, in order to interpret their propertiesand the function of hippocampal circuits.

Finally, in a second Review discussingthe role of grid cells in mammaliannavigation, Philippe Gaussier, affiliatedwith the École Nationale Supérieure del’Électronique et de ses Applications,France, describes how he and hiscolleagues use robots that are capable ofvisual learning and path integration tounderstand the role of the entorhinalcomplex – associated with thehippocampus in the mammalian brain – innavigation ( jeb186932). However, theteam challenges the role of grid cells inthe entorhinal complex in pathintegration, suggesting instead that thestructure is a generic merging toolthat builds a compact representation ofbrain activity in other regions implicatedin homing and dead-reckoning activities.

Human navigationHow our own navigational skills developand change as we age has long fascinatedpsychologists, and Nora Newcombe fromTemple University, USA, discusses howinfants and children build anunderstanding of the world around them( jeb186460). Explaining that thedevelopment of our ability to navigate istightly correlated with the emergence ofmotor skills and our developing senses,Newcombe describes how babies are ableto use external cues to learn where objectsare located, while toddlers can combineinformation about other objects in theenvironment to learn about theirsurroundings. Although children continuerefining their spatial awareness throughoutchildhood, they may not be able tocombine information from our differentsenses and systems in an optimal way untilthe ages of 10 or 11, and Newcombe addsthat our navigational skills are incompleteuntil around the age of 12.

Continuing the theme of humannavigation, Lucia Jacobs from theUniversity of California, Berkeley, USA,discusses the possibility that followingodours for navigation may have driven thedevelopment of the distinctive shape ofthe human nose ( jeb186924). Jacobssuggests that competition with othercarnivores led Homo sapiens to hunt over

A dung beetle rolling a dung ball along a straightlinewith the bearing shown on a compass. Photocredit: Chris Collingridge.

A sweat bee (Megalopta genalis), the speciesused by Stanley Heinze to delineate his pathintegration model of navigation. Photo credit:Ajay Narendra.

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long distances in groups before returningwith the prey. She explains that this wouldhave necessitated accurate spatialnavigation, which could have been mademore tractable by the development of stereoolfaction to allow the hunters to locateodours with more precision. However, sheadds that since the earliest humans migratedout of Africa there have been many moreadaptive pressures on the shape of the nose,accounting for the wide array of shapes thatwe see today.

In summaryHaving compiled this issue dedicated tonavigation in collaboration with hercolleagues, Webb and el Jundi, Kelbersays, ‘I think the collection provides across-section of study organisms, thehottest concepts and new methods thatwill take the field forward’, adding, ‘Foranyone interested in the broad topic ofanimal navigation and its physiologicalbasis, this is better than any textbook. It’s amust-read’. And she is excited about the

future. ‘I have two candidates for the nextbig discovery’, she says: ‘One isunravelling the genetic code for spatialnavigation… the other is finding thesensory basis of the magnetic sense thatallows animals to find their way’.Whichever wins out first, it is certainlygoing to be a gripping race.

10.1242/jeb.199752

Kathryn Knightkathryn.knight@biologists.com

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