Current Biology Vol16No5

R152
Primer
Ants
Philip S. Ward
Antsareoneofevolutionsgreat
successstories.Arisinginthe
mid-Cretaceousabout120million
yearsago,theynowcomprisea
diverseassemblageof
approximately20,000speciesand
havecolonizedmostofthe
worldsterrestrialbiomes.They
imposeastrongecological
footprintinmanycommunitiesin
theirvariedrolesasscavengers,
predators,granivores,and
herbivores.Insometropical
foreststhebiomassofants
exceedsthatofterrestrial
vertebratesbyafactoroffour,
andtheirsoil-turningactivities
dwarfthoseofearthworms.There
isawordforantinmost
languages,reflectingtheir
ubiquityanddistinctivenessto
humans.Theecological
dominanceandconspicuous
socialbehaviorofantshavelong
engagedtheattentionofnatural
historians.Intermsoftheir
speciesdiversity,relative
abundance,ecologicalimpact
andsocialhabits,antsemergeas
oneofthemostprominentgroups
ofarthropods.
Thereisimpressivebreadthin
theecologicalcharacteristicsof
antsandintherangeof
environmentstowhichtheyhave
adapted.Fromdesertstotropical
rainforests,fromgrasslandsto
mangroveswamps,most
terrestrialhabitatsaretenantedby
ants,andusuallyinmoderateto
highdensities.Antsareentirely
absentonlyfrompolarregions
andpoorlyinsolatedhighaltitude
locations(forexample,tropical
cloudforestsabove2400meters).
Nestsaresituatedinawide
varietyofsitesfromhighinthe
forestcanopytodeep
underground.Whilemostant
speciesarerathergeneralized
scavengers,othershavebecome
specializedpredators,seed-
harvesters,andfungus-growers.
Manyspeciesavidlytend
honeydew-producing
hemipterans,imbibingliquids
processedthroughthegutof
theseplant-feedinginsects,and
therebyactingasindirect
herbivores(aswellasmutualists
withtheirhosts).
Alegionofotherarthropodshas
becomeintimatelyassociatedwith
antcolonies,exploitingtherich
concentrationofresources
therein.Relationshipsrangefrom
parasitictomutualistic.Oneofthe
morestrikingsymbiosesisthe
coevolvedassociationbetween
attineantsandcertain
Figure1.Inmostantspeciestheworkercasteismonomorphicasinthismyrmicine
ant,Monomorium sydneyense.Inthisspeciestheegg-layingqueen(rightofcenter)is
distinctlylargerthantheworkers,butinotherspeciesthedifferencesmaybeless
marked.Clustersofpalelarvaearealsovisible.PhotographcourtesyofAlexWild
(www.myrmecos.net).
basidiomycetefungiwhichthey
cultureintheirnests.This
relationshipisnowknownto
involveadditionalparticipants,
includingamutualisticbacterium
thathelpstheantssuppress
unwantedparasiticfungi.
Mutualisticinteractionsbetween
antsandvascularplantsarealso
common,withmanyplants
supplyingrewardstoantsinthe
formoffoodand/orshelterin
returnforprotectionagainst
herbivores.
Nearlyallantspeciesare
eusocial,thatis,theylivein
perennialcolonieswith
overlappinggenerations,
cooperativecareofthebrood,and
cruciallyreproductive
divisionoflabor,suchthatmost
colonymembersbelongtoanon-
reproductive(worker)caste.The
onlyexceptionsareafewsocially
parasiticspecieswhichhave
secondarilylosttheworkercaste
andrelyonlaborsuppliedby
workersoftheirhostants.Itis
reasonabletoassumethatthe
mostrecentcommonancestorof
antswaseusocial,andthat
subsequentevolutionhasinvolved
elaborationsofthattrait.Thisisin
contrasttobeesandwaspsin
whichworker-basedsocieties
haveevolvedseveraltimesfrom
solitaryancestors.
Becausetheyarefullysocial,
antsdonottellusagreatdeal
aboutthetransitionfromsolitary
toeusocialbehavior.Nevertheless
theontogenyofantcolonies
withqueensofmostspecies
foundingcoloniesontheirown
andsingle-handedlyrearingthe
firstbroodofworkerssuggests
thateusocialityinantswas
achievedviatheso-called
subsocial route,inwhich
extendedparent-offspringcontact
ledtooverlapofgenerationsand
wasthenfollowedbytheoriginof
non-reproductiveworkers.
Regardlessofthedetailsofthis
sequenceofevents,whichof
coursewasplayedoutlongago,
contemporaryantsofferabundant
opportunityforcomparative
studiesofcolonylifeafterthe
eusocialthresholdhasbeen
crossed.Thereissubstantial
variationamongantspeciesin
suchtraitsasthenumberof
queenspercolony,mating
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frequency,sexratio,male
parentageandtheextenttowhich
workersandqueenshave
divergedmorphologicallyand
behaviorally.Thisprovidesfertile
materialforstudiesofintra-colony
conflict,casteevolutionandother
aspectsofadvancedeusociallife.
Forreasonsthatarenotfully
understoodthereareremarkable
discrepanciesinthecomplexityof
colonyorganizationamong
differentgroupsofants.The
popularimaginationisexcitedby
storiesofarmyants,leaf-cutter
ants,mound-buildingwoodants
andotherspecieswithpopulous
colonies,denseforagingtrails,
specializedworkersubcastesand
complexsystemsofchemical
communication.Yetatthesame
timemanyantspecies,occurring
inthesamecommunitiesasthese
ecologicaldominants,havesmall
colonysizes,showlimitedworker-
queendifferentiation,andexhibit
muchmoremodestcapabilitiesof
foraging,recruitmentand
communication.
Despiteapparentadvantagesat
thecolonylevelofhaving
speciallyadaptedworker
subcastes,mostspeciesofants
haveworkersthatare
morphologicallyuniforminsize
andshape(Figure1).Onlya
minorityofantspecieshave
workerswithpronounced
polymorphism(Figure2),although
adivisionoflaborbasedonageis
nearlyuniversal.Thepointto
emphasizeisthatsincetheir
divergencefromacommon
ancestorintheCretaceous,some
antlineagessuchastheiconic
armyantsandleaf-cuttingants
haveevolvedquitecomplex
societieswhileothers,suchasthe
primitivebulldogantsof
Australia,haveremainedata
muchlessadvancedlevel.The
factorsresponsibleforsuch
heterogeneityintherateofsocial
evolutionhavebeenlittle
explored,andwillrequireacareful
analysisofecologicaland
phylogeneticinfluences.
Hymenopteran heritage
Antsaretreatedasasinglefamily,
Formicidae,intheorder
Hymenoptera,alargeanddiverse
groupofholometabolousinsects.
Theearliesthymenopteranswere
Figure 2. An example of
worker polymorphism in
ants. In these workers of
Camponotus sansabeanus
thereisdistinctvariationin
sizeandbodyproportions,
especially head shape.
Since the workers are
geneticallysimilarsuchvari-
ation reflects the outcome
ofdivergentdevelopmental
pathways. Photograph
courtesyofAlexWild.
herbivores,withcaterpillar-like
larvaethatfedonplanttissues.
Someofthesephytophagous
lineagessurvivetothepresent
day.Butmostextant
Hymenopteraareparasitoidsor
predatorsbelongingtoa
distinctivecladeknownasthe
Apocrita,inwhichthefirst
segmentoftheabdomenhas
becomefusedtothethorax,and
isseparatedfromtheremainder
oftheabdomenbyastrong
constriction.Morphologistsuse
thetermtagma (pluraltagmata)to
refertoafunctionallyintegrated
setofbodysegments.Insectsare
classicallyconsideredtohave
threetagmata:head,thoraxand
abdomen.ApocritanHymenoptera
exhibitauniquereorganizationof
thebodypartsinwhichthe
middletagmaiscomposedofthe
thoraxplusabdominalsegment1,
whiletheposteriortagma
comprisestheremaining
abdominalsegments.Itisunclear
howthisevolutionarynovelty
arose,butoneapparent
consequenceisthatadditional
constrictions,involvingabdominal
segments24,evolvedinsome
apocritans,givingthem
exceptionaldexterityof
abdominalmovement.
Thistakesonadded
significancewhenweconsider
anotherimportantdevelopment
thatoccurredwithinonegroupof
Apocrita:theovipositorwas
modifiedintoastingingdevice,
usedtoinjectparalyzingvenom
intohostsorprey.Thestingalso
becameapotentdefensive
weaponinthosespeciescaring
foryounginanest.Thestinging
Hymenoptera,orAculeata,
includebothparasitoidsand
predators,butthelatterare
predominantandshowan
illuminatingarrayofnesting
behaviors.Somespeciessimply
cachepreyitemsinacrude
cavity,layeggsanddepart,while
othersconstructnestsofvarying
degreesofelaboration,
sometimesprovidingparental
careofoffspring.Itiswithinthis
groupofnesting,stinging
Hymenopterathatantsevolved.
Anotherimportantheritagethat
antssharewithallother
hymenopteransishaplodiploidy,a
geneticsysteminwhichmalesare
haploidandarisefromunfertilized
eggs,whilefemalesarediploid
anddevelopfromzygotes.
Haplodiploidyyieldsunusual
asymmetriesofgenetic
relatedness,withfemalesbeing
morecloselyrelatedtotheir
sisters(0.75)thantotheirbrothers
(0.25).Ithasbeenproposedthat
thisunderpinsauniversalfeature
ofsocialhymenopterans:the
workersarefemaleonly,with
malesshowinglittleornohelping
behavior.Thisisincontrasttothe
othermajorgroupofeusocial
insects,thediploidtermites,in
whichworkersaredrawnfrom
bothsexes.Anadditional,and
perhapsco-acting,constrainton
maleaculeatehymenopteransis
thattheydonotpossessasting,
limitingtheirabilitytoadopt
worker-likeroles.
Antsdifferfromsocialbeesand
waspsinoneimportantrespect:
theworkersofantsareentirely
wingless.Thisplacesconstraints
ontheirforagingbehaviorandhas
probablyspurredtheevolutionof
complexchemicalcommunication
systems,suchastrailand
recruitmentpheromones,designed
forterrestrial(asopposedtoaerial)
movement.Italsomakesthe
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analogybetweenantcoloniesand
perennialplantsespeciallystriking.
Botharelong-lived,sessile
organismsthatarelimitedspatially
intheirabilitytoreachoutand
procureresources.Additional
similaritiesincludetheirmodular
construction(referringtocolonies,
notindividualants),phenotypic
plasticity,andvariedchemical
strategiesforterritorialdefense.
Origin of ants
Thereislittledoubtthatantsarea
monophyleticgroup.Theysharea
distinctivesuiteofmorphological
features,includinggeniculate
(elbowed)antennae,aprognathous
(forward-projecting)head,a
characteristicconfigurationofthe
foretibialantennacleaner,
modificationofthesecond
abdominalsegmenttoforma
node-likepetiole,andseveral
uniqueexocrineglands.Yetthe
closestlivingrelativesofantshave
notbeenunequivocallyidentified.
Severalotherfamiliesofaculeate
Hymenoptera,inasubgroup
knownastheVespoidea,have
beentoutedaspossiblesister
groupsofantsincludingTiphiidae,
Bradynobaenidaeandthe
combinationofVespidaeplus
Scoliidae.Itisameasureofthe
incompletenessofour
phylogeneticknowledgethatnone
ofthesealternativeshas
particularlystrongsupport.In
manyrespectsthesummary
cladogrampublishedbyFredrik
Ronquistin1999,whichdepicted
mostvespoidfamiliesemerging
outofanunresolvedbush,still
appliestoday.
Thefossilrecordhelpsto
explainthisimpasse.Most
familiesofaculeatewaspsappear
rathersuddenlyintheearly
Cretaceous,suggestingthatthere
Figure 3. A predatory
poneroidant.Theworkers
of this species, Amblyo-
pone oregonensis, prey
largely on geophilomorph
centipedes. Photograph
courtesyofAlexWild.
Cretaceousdeposits,andare
consideredtobeearlystem-
groupformicids,probablythe
nextclosestrelativesofcrown-
groupantsafterthe
sphecomyrmines.
The ant tree of life
Onemightexpectthatthe
phylogeneticrelationshipsamong
livingrepresentativesof
Formicidaehavebeenreasonably
wellclarified.Infactmany
uncertaintiespersistheretoo,and
thisisanareaofactive
investigationanddebate.
Morphologicalstudieshavebeen
helpfulincircumscribingthemajor
lineages(subfamilies)ofants,but
therelationshipsamongthem
havelargelyeludedconfident
resolution.
Moleculardata,intheformof
DNAsequencesfrommultiple
nucleargenes,arejustnowbeing
appliedtotheproblem.Suchdata
confirmthemonophylyofnearly
allofthesubfamilies,butthey
alsorevealanumberofnoveland
unexpectedgroupings.For
example,mostantsbelongtoa
wellsupportedclade,the
formicoidgroup,whichcontains
about90%ofalllivingantspecies
andencompasses14ofthe20
extantsubfamilies.Mostants
encounteredbythecasualhuman
observerbelongtothisgroup.Itis
uncleariftheremaininglineages
theso-calledponeroidsare
acladeoragrade.Thatistosay,
theymightformtheirownunitary
lineageor,morelikely,they
representthegroupwithinwhich
theformicoidsoriginated.Manyof
theponeroids(Figure3)are
consideredtohaveundergone
lessmorphologicalandbehavioral
changethanotherants,butsome
formicoids(suchastheafore-
mentionedbulldogants,subfamily
Myrmeciinae)retainrelatively
simplecolonystructureand
communicationsystemsaswell.
Anotherinsighttoemergefrom
molecularphylogeneticanalyses
ofantsisthattherehasbeen
profoundmorphological
convergenceinsomeaspectsof
workermorphology,totheextent
thatitmisledearlierphylogenetic
inferences.Forexample,a
constrictionbetweenabdominal
segments3and4,andthe
wasarapidburstofdiversification
oncethestinghadevolved.Ants
maketheirappearancealittle
later,about100millionyearsago.
Thefirstdiscoveredandmost
famousofCretaceousantsis
Sphecomyrma,describedalmost
40yearsagofromtwowonderfully
preservedworkerspecimensin92
million-year-oldNewJersey
amber.Sphecomyrma bearsa
tantalizingmixofant-andwasp-
liketraits.Infactitexhibitsmost,
butnotall,ofthediagnostic
featuresofmodernants,
indicatingthatitisastem-group
formicid.Inotherwords,itismore
closelyrelatedtoantsthantoany
otherextantorganisms,butthe
mostrecentcommonancestorof
livingantsandtheirdescendants
(thecrown-group formicids)are
morecloselyrelatedtoone
anotherthantoSphecomyrma.
Amoreextensiveseriesoffossil
antshasnowbeendocumented
fromtheCretaceous.Thefossils
rangeinagefromabout78to100
millionyears,andtheyinclude
someundoubtedcrown-group
taxa.Amongthemorespectacular
findsareadditionalwellpreserved
specimensfromNewJersey
amber,includingrepresentatives
ofthemodernsubfamily
Formicinae,aswellasfossilsfrom
Canada,Eurasia,andsouthern
Africa.Thistaxonomicdiversity
andgeographicspreadindicates
thatcrown-groupantsarose
sometimebeforethisperiod,
perhapsaslongagoas120
millionyears.Theprevalenceof
northernhemispherefossils
suggestsanorigininthenorthern
supercontinentofLaurasia,
followedbydispersalto
Gondwana.Ant-likefossilsplaced
intheextinctfamilyArmaniidae
areknownfirstfromnorthernmid-
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formationofasecondnode-like
structure(apostpetiole),has
evolvedrepeatedlyinants.Some
subfamilieswhichsharethis
characteristic,suchasthe
formicoidMyrmicinaeandthe
poneroidAgroecomyrmecinae,
hadbeenplacederroneously
togetherinearliermorphology-
basedstudies.
Thenewphylogenetic
estimates,combinedwithfossil-
calibratedmoleculardating
analyses,suggestthatthehistory
ofantsinvolvesaseriesof
sequentialdiversifications:
evolutionofsphecomyrmineand
poneroid-likelineagesintheearly
Cretaceous,about100120million
yearsago,followedbyamore
exuberantdiversificationof
formicoidsbeginningabout100
millionyearsagoandcontinuing
intothePaleogene.Thefossil
recordprovidessomeadded
perspective:eventhoughthe
moleculardataindicatethatmost
ofthemajorlineagesofants
(subfamilies)aroseinthelate
Mesozoic,antsaresparseas
Cretaceousfossils,makingup
lessthan1%ofallinsect
specimens.Theyshowamarked
increaseinabundancefromthe
Eocene(approximately50million
yearsago)onwardandcomprise
amuchlargerfractionofallinsect
fossilsfromtheselaterperiods.
MoreovermostoftheTertiaryant
fossilshavebeenassignedto
modern(extant)genera,while
noneoftheCretaceousfossils
hasbeensoclassified.Inshort,
whilethestemlineagesofmodern
antsubfamilieswerepresent
beforetheKTboundary,the
ecologicaldominanceandrange
ofdiversitythatweassociatewith
modernantsdidnotariseuntil
laterintheTertiary,about6070
Figure 4. Aphid-tending
formicoid ants. These are
workers of Formica aerata,
guarding aphids on willow.
PhotographcourtesyofAlex
Wild.
explanationsfortheirascendancy.
Akeychangethatoccurredinthe
Cenozoicwasanexpansionand
modificationofdietfromthe
originalpredatoryhabitsthatants
inheritedfromtheiraculeate
forebears.Inparticularantsbegan
toexploittherichcarbohydrate
resourcesavailableintheformof
honeydewsecretedbyplant-
feedinghemipterans(Figure4).
Othersbecamespecializedas
seed-harvestersand(inone
instance)fungus-cultivators.
Thesedietaryshiftsoccurred
multipletimesbutwererestricted
almostexclusivelytothe
formicoids.Forthemostpartthe
poneroidlineagesretainedtheir
predatoryways.Sothesuccessof
antsrestslargelyontheshoulders
oftheformicoids.Onecanimagine
thatifformicoidshadnotevolved,
antswouldbeperceivedasa
modestgroupoftropicalwingless
wasps(withnovernacularterm
reservedforthem),asopposedto
thenear-ubiquitousecological
dominantsthatweknowtoday.
But,thenagain,maybeanother
poneroidwouldhavesteppedinto
fillthevoid.
Further reading
Bolton,B.(2003).Synopsisandclassification
ofFormicidae.Mem.Am.Entomol.Inst.
71,1370.
Bourke,A.F.G.,andFranks,N.R.(1995).
Socialevolutioninants.(Princeton:
PrincetonUniversityPress).
Davidson,D.W.,Cook,S.C.,Snelling,R.R.,
andChua,T.H.(2003).Explainingthe
abundanceofantsinlowlandtropical
rainforestcanopies.Science300,
969972.
Grimaldi,D andAgosti,D.(2000).A
formicineinNewJerseyCretaceous
amber(Hymenoptera:Formicidae)and
earlyevolutionoftheants.Proc.Natl.
Acad.Sci.USA97,1367813683.
Hlldobler,B.,andWilson,E.O.(1990).The
ants.(Cambridge,Massachusetts:
HarvardUniversityPress).
Ronquist,F.(1999).Phylogenyofthe
Hymenoptera(Insecta):thestateofthe
art.Zool.Scr.28,311.
Ward,P.S.,Brady,S.G.,Fisher,B.L.,and
Schultz,T.R.(2005).Assemblingtheant
TreeofLife(Hymenoptera:
Formicidae).Myrmecol.Nachr.7,8790.
Wilson,E.O.,andHlldobler,B.(2005).The
riseoftheants:aphylogeneticand
ecologicalexplanation.Proc.Natl.Acad.
Sci.USA102,74117414.
DepartmentofEntomologyandCenter
forPopulationBiology,Universityof
CaliforniaatDavis,OneShieldsAvenue,
Davis,California95616,USA.E-mail:
psward@ucdavis.edu
millionyearsafterantsfirst
evolved.
Why are ants so successful?
Severalcommentatorshave
arguedcompellinglythatthe
socialbehaviorofantsis
responsibleatleastinpartfor
theirevolutionarysuccessand
ecologicaldominance.Eusociality
confersmarkedadvantagesin
termsofresourceacquisition,
defenseagainstenemies,and
bufferingofenvironmental
variation.Thedivisionoflaborand
flexibilityoftaskallocationthat
arethehallmarksofadvanced
socialinsectsenablethemto
meetcontingenciesandexploit
opportunitiesmuchmore
efficientlythansolitaryinsects.
Butthiscannotbetheentire
story.Evenamongsocialinsects
antsareespeciallynotablefor
theirabundanceanddiversity,so
additionalfactorsmustbe
invokedtoexplaintheirparticular
prominence.Onepossibilityis
historicalpreemption:thefossil
recordindicatesantswerethe
secondinsects(aftertermites)to
developeusociality,andthefirst
groupofpredaciousinsectstodo
so.Theymayhaveeffectively
occupiedmuchofthenichespace
availableforsocialinsect
predatorsjustas,inanearlier
phaseofearthhistoryandata
largerscale,thefirstcrustaceans
tocolonizelandancestorsof
todaysinsectsprobably
inhibitedlaterinvasionsof
terrestrialhabitatsbyother
crustaceans.
Finally,wehaveseenthatants
didnotachieveecological
dominanceuntil6070million
yearsaftertheyarose,soneither
eusocialitynorhistorical
precedencearesufficient