the evolution of agriculture in insects

38 Pages·2005·0.45 MB·English

20Oct2005 12:41 AR ANRV259-ES36-24.tex XMLPublishSM(2004/02/24) P1:OJO
10.1146/annurev.ecolsys.36.102003.152626
Annu.Rev.Ecol.Evol.Syst.2005.36:563–95
doi:10.1146/annurev.ecolsys.36.102003.152626
Copyright(cid:1)c 2005byAnnualReviews.Allrightsreserved
FirstpublishedonlineasaReviewinAdvanceonAugust19,2005
T E A I
HE VOLUTION OF GRICULTURE IN NSECTS
Ulrich G. Mueller,1,2 Nicole M. Gerardo,1,2,3
Duur K. Aanen,4 Diana L. Six,5 and Ted R. Schultz6
1SectionofIntegrativeBiology,UniversityofTexasatAustin,Austin,Texas78712;
g
or email:[email protected]
ws. 2SmithsonianTropicalResearchInstitute,Apartado2072,Balboa,RepublicofPanama
vie 3DepartmentofEcologyandEvolutionaryBiology,UniversityofArizona,Tucson,
e
alr Arizona85721-0088;email:[email protected]
nuy. 4DepartmentofPopulationBiology,BiologicalInstitute,UniversityofCopenhagen,
nals.anuse onl 25D10e0paCrotmpeennhtaogfeEnc,oDsyesntmemarakn;demCaoinl:[email protected],kUniversityofMontana,
ournal Missoula,Montana59812;email:[email protected]
m arjerso 6DepartmentofEntomology,NationalMuseumofNaturalHistory,
ded fro5. For p Semmaitihl:[email protected],dWuashington,DistrictofColumbia20013-7012;
a0
nlo14/
w1/
Don 1 KeyWords Attini,Macrotermitinae,mutualism,symbiosis,Xyleborini
63-595. Austin o a■ntsA,bosntcreacitn teArmgriitceusl,tuarnedhsaesveevnoltvimedesinidneapmenbdreonstilaybienetthlerse.eAinlstheoctugohrdtehres:seonincseeicnt
st. 2005.36:5y of Texas - faafaarsrremmcrleeeomrrnsagalaerkrnmeaeborianlnytoisocsoniummslteiualsrawerw,sasyewulslgi.tqghLueionsittneitgnhd-getieifcrfroemnnreevcnselttrosgfnearaonnlmtdme,veoionanlcoumhctiuooolstntthu.ercAera,lsplienrpse,rsmoecpanloantsngyaaslmtpleyeotchraieaeclirwropcasrsuyolsbmtiltveahmaneryyss
ol. Syversit fordiseasecontrol,butinsectfarmershaveevolvedacombinationofstrategiestoman-
EvUni agecropdiseases:They(a)sequestertheirgardensfromtheenvironment;(b)monitor
Ecol. by aglalrydeancsceisnstepnospivuellayt,iocno-nletrvoelllirnegsepravtohiorsgeonfsgeeanrelyticianlldyisveaarsieaboluetbcruelatikvsa;rs(,c)evoecncawsihoinle-
v. propagatingclonalmonoculturesacrossmanyfarmergenerations;and(d)manage,in
e
R
u. additiontotheprimarycultivars,anarrayof“auxiliary”microbesprovidingdisease
nn suppressionandotherservices.Ratherthangrowingasinglecultivarsolelyfornutri-
A
tion,insectfarmersappeartocultivate,andpossibly“artificiallyselect”for,integrated
crop-microbeconsortia.Indeed,cropdomesticationinthecontextofcoevolvingand
codomesticatedmicrobialconsortiamayexplainthe50-millionyearoldagricultural
successofinsectfarmers.
1.INTRODUCTION
The cultivation of crops for nourishment has evolved only a few times in the
animal kingdom. The most prominent and unambiguous examples include the
fungus-growing ants, the fungus-growing termites, the ambrosia beetles and, of
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564 MUELLERETAL.
course,humans.Forhumans,whostartedthetransitionfromanancestralhunter-
gathererexistencetofarmingonlyabout10,000yearsago(Diamond1997,Smith
1998), sustainable, high-yield agriculture has become critical for survival in a
globaleconomywithprojectedfoodshortages,anddiverseresearchprogramsare
currentlydevotedtotheoptimizationofagriculturalproductivityinthecontextof
growingenvironmentalchallenges(Greenetal.2005).Agriculturalprogresshas
beenachievedbyhumansthroughacombinationofinsight,creativeplanning,and
a fair share of contingency and luck (Diamond 1997, Schultz et al. 2005, Smith
1998).However,humanshavesofarnotexaminednonhumanagriculturalsystems,
org suchasthefungus-growinginsects,forpossibleinsightstoimproveagricultural
ws. strategies.
e
vi This lack of an applied interest in insect agriculture probably derives from a
e
alr general perception that human agricultural systems (based largely on plant cul-
als.annuse only. tbiavsaetidono)nffuunncgtiuosnciunltiavaftuinodna).mHeonwtaellvyerd,ihffuemreanntsmhaanvneelreathrnanedinmseuccthsoyfstpermacsti(caalll
nu
ournal valuethroughthecloseexaminationofadaptivefeaturesofotherorganisms(in-
arjso cludinginsects),andcomparableproblemssuchascropdiseasesaffectallfarmers
d from For per roergoatrhdelerwssisoef).thBeeircapuhsyeloogfentheeticunpiovseirtsioalnistyoorfthcorsoepodfistehaesirescrionpbso(tphlahnut,mfaunngaunsd,
ade05. insectagriculture,itmaybefruitfultoexaminetheshort-termandlong-termsolu-
nlo14/ tionsthathaveevolvedconvergentlyininsectagricultureforpossibleapplication
w1/
Don 1 to human agriculture (Denison et al. 2003). Such a synthesis is the goal of this
3-595. ustin o review.
6A
005.36:5Texas - 1D.1efi.BnienhgavAigorriaclualntudreNutritionalElements
st. 2y of
Sysit Insectfungicultureandhumanfarmingsharethedefiningfeaturesofagriculture
ol. ver (see Table 1): (a) habitual planting (“inoculation”) of sessile (nonmobile) cul-
EvUni tivars in particular habitats or on particular substrates, including the seeding of
col. by new gardens with crop propagules (seeds, cuttings, or inocula) that are selected
E
v. bythefarmersfrommature(“ripe”)gardensandtransferredtonovelgardens;(b)
e
u. R cultivationaimedattheimprovementofgrowthconditionsforthecrop(e.g.,ma-
nn nuring;regulationoftemperature,moisture,orhumidity),orprotectionofthecrop
A
againstherbivores/fungivores,parasites,ordiseases;(c)harvestingofthecultivar
for food; and (d) obligate (in insects) or effectively obligate (in humans) nutri-
tionaldependencyonthecrop.Obligatedependenciesoftheinsectfarmerscanbe
readilydemonstratedbyexperimentalremovaloftheircultivatedcrops,resulting
in reduced reproductive output, increased mortality, or even the certain death of
thecultivar-deprivedinsect(Francke-Grosmann1967,Grasse´ 1959,Norris1972,
Sands1956,Weber1972).Ourdefinitionofagriculturedoesnotrequireconscious
intentinplantingandharvesting.Consciousplanning,learning,andteachinghave
clearly accelerated the development of complex agriculture in humans, but pre-
sumablynotininsects(Schultzetal.2005).
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EVOLUTIONOFAGRICULTUREININSECTS 565
e
Humans Facultativ Present Present Absent Present Present Present Present Present 1Absent Social Present Present Present
sia 2unal
o m
r
b m
m o
a c
nualreviews.orgy. urein: Xyleborinebeetles Obligate Present Present Present Present Present Unknown Unknown Unknown Unknown Subsocialor Present Unknown Absent
als.anse onl ricult
Annu. Rev. Ecol. Evol. Syst. 2005.36:563-595. Downloaded from arjournby University of Texas - Austin on 11/14/05. For personal u TABLE1Agriculturalbehaviorsoffarmingants,termites,beetles,andhumans Ag MacrotermitineAgriculturalbehaviorAttineantstermites DependencyoncropforfoodObligateObligate Engineeringofoptimalgrowthconditionsforcrop(e.g.,PresentPresentsubstratepreparation;moistureorhumidityregulation) PlantingofcroponimprovedsubstratePresentPresent Intensive,continuousmonitoringofgrowthanddiseasePresentPresentstatusofallcrops SustainableharvestingofcropforfoodPresentPresent ProtectionofcropfromdiseasesandconsumersPresentPresent WeedingofalienorganismsinvadingthegardenPresentPresent UseofchemicalherbicidestocombatpestsPresentUnknown UseofmicrobialsymbiontsfornutrientprocurementforPresentUnknownthecrop Useofdisease-suppressantmicrobesforbiologicalPresentUnknownpestcontrolSocialityStrictlyeusocialStrictlyeusocial TaskpartitioninginagriculturalprocessesPresentUnknown ApplicationofartificialselectionforcropimprovementUnknown,butantsUnknownexertsymbiontchoice LearningandculturaltransmissionofagriculturalAbsentAbsentinnovations 1SeeSection7forsomerecentlydiscoveredmicrobeswithpotentialdisease-suppressantproperties. 2Oneambrosiabeetlespeciesiseusocial,allotherspeciesappeartobesubsocialorcommunal(seetext).
20Oct2005 12:41 AR ANRV259-ES36-24.tex XMLPublishSM(2004/02/24) P1:OJO
566 MUELLERETAL.
Werestrictourreviewtoant,termite,andbeetlefungiculturists.Casesanalo-
goustohumananimalhusbandry,suchasthetendingbyantsofhemipteraninsects
(e.g.,aphids,treehoppers;Ho¨lldobler&Wilson1990),arebeyondthescopeofthis
review.Wealsoexcludecasesthatfailtomeetallfouroftherequirementsofagri-
cultureasdefinedabove,including,e.g.,theantLasiusfuliginosus,whichpromotes
fungalgrowthinthewallsofitsnest,becausethefungusisapparentlynotgrownfor
foodbutinsteadforstrengtheningthewalls(Maschwitz&Ho¨lldobler1970)orfor
antibioticprotectionofthewalls(Mueller2002).Onthesamegrounds,weexclude
a number of possible cases of incipient agriculture. For example, Littoria snails
org may“protofarm”fungibycreatingplantwoundsthatbecomeinfectedwithfungal
ws. growththatispartofthesnails’diet,butthesnailsdonotactivelyinoculatethe
e
vi plantwoundsorotherwisegardenthefungi(Sillimanetal.2003).Manymoresuch
e
alr protofarmingspeciesprobablyawaitdiscovery,particularlyamonginvertebrates,
als.annuse only. atlneds)apllroofbathbelyknooriwgniniantseedctfraogmriccuoltmurpiasrtsab(fleunpgruosto-gargorwiciunlgtuarnatlsa,ntecremstioterss,(aMndueblelee-r
nu
ournal et al. 2001, Schultz et al. 2005). Comparison of these protofarming insects with
arjso “primitive”humanagricultureexceedsthescopeofthisreview.
m er
d froFor p
de5. 1.2.ACoevolutionaryApproachto
a0
nlo14/ UnderstandingAgriculture
w1/
o1
3-595. Dustin on Wbyetwheillnauntariltyizoenaalgraincdultbuerheaavsioartaylpceroitfesritarosnugmcmoeavroizluetdioanbaoryvei,ntienrawcthioicnh,dneafitunreadl
6A selection acts upon both farmers and crops as reciprocally interdependent lin-
005.36:5Texas - eaaggriecsul(tFuuretucyomnasi&derSslantoktinon1l9y8t3h,eRiinntderoasct1i9o8n4s)b.eOtwureecnoeavospluetciiofincarfyarampipnrgoainchsetcot
st. 2y of and a single cultivated crop, but also its interactions with other pathogenic and
Sysit mutualistic microbes that have recently been discovered in insect gardens. Like
ol. ver thecultivars,someofthesemicrobesarealsomanagedbytheinsectfarmersfor
col. Evby Uni stupreec,ibfiuctpausrepqouseesst(eFriegduarend1)e.nIgnionteheerrewdoercdosl,oagnicianlsceoctmgmarudneintyiscnoontsaisptiunrgemofosneovceural-l
E
v. interacting microbes, some beneficial and others detrimental to the farmers. To
e
R
u. gainacomprehensiveunderstandingoftheprinciplesofinsectagriculture,itwill
nn thereforebenecessarytoexaminethenatureofinsect-microbeinteractionsingar-
A
dens,theevolutionaryoriginsoftheseinteractions,andtheconvergentanddiver-
gentevolutionarytrajectoriesthatculminatedintheextantagriculturalsystemsof
insects.
2.THETHREEINSECT-AGRICULTURESYSTEMS
Behaviorally complex systems of insect agriculture are known from only three
groupsofinsects:ant,termites,andbeetles.
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EVOLUTIONOFAGRICULTUREININSECTS 567
2.1.AntFungiculture
The fungus-growing ants are a monophyletic group of about 220 described and
manymoreundescribedspeciesinthetribeAttini(subfamilyMyrmicinae)(Price
et al. 2003, Schultz & Meier 1995). Attine ants occur only in the New World
(ArgentinatothesouthernUnitedStates)andattaintheirgreatestdiversityinthe
wetforestsofequatorialSouthAmerica,theregionoftheirpresumedevolutionary
origin(Muelleretal.2001).Attineantsareobligateagriculturists;theircultivated
fungiarethesolesourceoffoodforthelarvaeandanimportantsourceoffoodfor
g theadults.Althoughadultsareabletosupplementtheirdietsbyfeedingonplant
s.or juices (Bass & Cherrett 1995, Murakami & Higashi 1997), the cultivated fungi
w
e are nutritionally sufficient to support the ants even in the absence of additional
vi
alre nutrients(Mueller2002,Muelleretal.2001).Gardenfungiaretransmittedverti-
nuy. callyacrossgenerationswhendaughterqueenstransportsmallpelletsofnatal-nest
nals.anuse onl mallyacneltisu(mFewrnita´hnidnetzh-eMirairn´ınfreatbualc.c2a0l0p4o,cHkeutbs,erpo1u9c0h5e,sMpureeslleenrt2in00t2h)e.mInotuhtehpdaerrtisveodf
ournal leafcutterants,theworkersaredividedintoaremarkablerangeofdifferentlysized
arjso
m er morphologicalcastes,eachspecializedonadifferenttask(Hartetal.2002,Weber
d froFor p 1972)(Figure2d).
de5. Different attine ant lineages cultivate their fungi on different substrates. The
a0
nlo14/ ancestralgardeningsubstrate,stillusedbytheso-calledlowerattines,consistsof
ow11/ flowerparts,arthropodfrass,seeds,woodfragments,orothersimilarplantdebris,
3-595. Dustin on lweahveeresaasntdheflolweaefrcsu.tDtinegspgiteentehreaseAtdtiastainncdtsAucbrsotmraytremsepxecpiarilmizaatriiolynsu,saellfarettsihnleysycus-t
6A temscontainatleastfoursymbionts:(a)thefungus-growingants;(b)theirfungal
005.36:5Texas - cMuulteivllaerrse(tbaasl.id1io9m98y,cMeteusnkinacthsieemtuaslh.r2o0o0m4)f;a(mc)ilimesutLueapliisottiaccaenaetibainodtiPc-tperruoldaucceianeg;
st. 2y of actinomycetebacteria(familyPseudonocardiaceae;Currieetal.1999b);and(d)
Sysit gardenparasitesintheascomycetefungalgenusEscovopsis(Currieetal.1999a,
ol. ver Currie et al. 2003b). Additional bacteria and yeasts also occur in attine gardens
Ecol. Evby Uni a(Cndarmreairyofeutnaclt.io1n99a7s,mCurtauvaelnisetst,ael..g1.,9b7y0,sSecarnettoinsgetdaigl.e2st0i0v4e)e.nzymesorantibotics
v.
e
R
u. 2.2.TermiteFungiculture
n
n
A
Ofthemorethan2600describedtermitespecies,about330speciesinthesubfamily
Macrotermitinae cultivate a specialized fungus, genus Termitomyces, for food.
Nestsaregenerallyfoundedbyasinglepairofreproductives,thefuturequeenand
king.Theysealthemselvespermanentlyinacellofhardclay(theso-calledroyal
chamber)wheretheyrearthefirstbroodofsterileworkers.Inmosttermitespecies,
anewcolonyacquiresafungalstrainfromwind-dispersedsexualTermitomyces
sporesshortlyafternestfoundingandbeginsconstructionofthefirstgardens(De
Fine Licht et al. 2005). These spores come from fruiting bodies (mushrooms)
thatarisefrommaturetermitecolonies.Thefruitingofthefungusappearstobe
roughlysynchronizedtotheperiodwhenthefirstforagingworkersemergefroma
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568 MUELLERETAL.
newnest,afewmonthsafterthenest-foundingstage.Termitegardensaregrown
ondeadplantmaterialthatisonlypartiallydecomposed,suchasleaflitter,dead
grass,deadwood,ordryleaves.
Termitegardensarebuiltfromspore-containingfecalpelletsinchambersthat
thetermitesconstructeitherinsideamoundordispersedinthesoil.Fecalpelletsare
addedcontinuouslytothetopofthecombandfungalmyceliumrapidlypermeates
thenewsubstrate(Figure2e).Afterafewweeks,thefungusstartstoproduceveg-
etativenodulesthatareconsumedbythetermites.Thesenodulesarearichsource
ofnitrogen,sugars,andenzymes.Thenodulesarealsocoveredwithindigestible
org asexual spores (conidia), so that consumption serves the additional function of
ws. inoculatingthefeceswithspores,whichpassthroughthegutunharmedandare
e
vi then planted in new comb with the deposition of feces (Leuthold et al. 1989).
e
alr Maturecombisalsoconsumed(Darlington1994),butitisnutritionallyinferior
als.annuse only. tothenodules.
ournnal u 2.3.BeetleFungiculture
m arjerso Ambrosiabeetlesmakeuparound3400ofthe7500speciesintheweevilsubfam-
ded fro5. For p iPlylatSycpooldyitninaaee;(Ftahrereblalrektaanl.d2a0m0b1r,oHsiaarrbineegttloens,2in0c0l5u,dWinogotdhe1t9r8a2d)it.ioMnoaslltyasmebpraorastiea
nloa14/0 beetles construct tunnel systems (galleries; Figure 2f) in woody tissues of trees
w1/ (typicallyinweakenedorrecentlydeadtreesor,morerarely,invigoroushosts),
o1
63-595. DAustin on apculetlthtiioovulaegtsehd(sHboaymrrtehinsegpbteoecenietls2e0sa0roe5n,sgpWaelcolieoardlyiz1we9da8ltl2os),.cuoTplhooenniwzteehrmpicithhatm,hlaebyrrgofeseiesaederaedsfse,arfnsruetxiotcstl,huaesnivdfuel,neogafri
005.36:5Texas - nfreoamrewxhcliuchsitvhee,yfoaocqdusioreurecses.eTnthiaelbveietatlmesinasr,eaombilnigoaatceildysd,aenpdensdteernotlsup(Boneatvheerf1u9n8g9i,,
st. 2y of Koketal.1970).
Sysit The most advanced fungiculturists among the ambrosia beetles occur in the
ol. ver Xyleborini,alargemonophyletictribeofabout1300species(Farrelletal.2001,
EvUni Jordal2002).Itisthisgroupofambrosiabeetlesthatweprimarilyfocusoninthis
col. by review.AlthoughlifehistoriesamongtheXyleborinivaryconsiderably,mostshare
E
v. anumberoffungiculturalcharacteristics.Thereisasexualdivisionoflaborinthe
e
u. R Xyleborini;onlyfemalesperformgardeningtasks,whereasmalesareshort-lived
nn andflightless(Norris1979).Aftermating,femalesdispersetonewhostsubstrate,
A
carrying the fungi in specialized pockets termed mycangia. Once within a new
host, founding females “plant” the fungi on the walls of the excavated tunnels,
layeggs,andtendtheresultinggardenandbrood(Norris1979).Inwaysnotfully
understood,theyareabletocontrolthegrowthofthefungalcrop,aswellas,to
adegree,thecompositionofitsmultiplefungalspecies(Beaver1989,French&
Roeper1972,Kingsolver&Norris1977,Roeperetal.1980).Ifthefemaledies,the
gardenisquicklyoverrunbycontaminatingfungiandbacteria,whichultimately
resultsinthedeathofthebrood(Borden1988,Norris1979).
Theambrosiagardensofxyleborinebeetlesarenotpuremonoculturesaswas
once believed, but are typically composed of an assemblage of mycelial fungi,
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EVOLUTIONOFAGRICULTUREININSECTS 569
yeasts, and bacteria (Batra 1966, Haanstadt & Norris 1985). These assemblages
weretermedmulti-speciescomplexesbyNorris(1965),whosuggestedthatitisa
complexasawhole,ratherthananyoneindividualmicrobe,thatallowsthebeetles
toexploitnutrient-poorsubstratessuchaswood.However,mostsubsequentwork
hasrevealedthatone“primary”fungusalwaysdominatesinbeetlegardens(Baker
1963,Batra1966,Gebhardtetal.2004,Kinuura1995).Furthermore,thebeetles
typically carry only the primary fungus in the mycangium (although secondary
fungi are sometimes also isolated from mycangia), and the cultivation efforts of
female beetles tend to favor the primary fungus, which imparts the greatest nu-
org tritional benefit (Francke-Grosmann 1967, Gebhardt et al. 2004, Morelet 1998,
ws. Norris1979).Someauxiliaryfungialsosupportbeetledevelopment,butsurvival
e
vi ontheauxiliaryfungialoneisoftengreatlyreduced(Norris1979).Theseobser-
e
alr vationsimplicatetheprimaryfungusastheintendedcrop,whereasthesecondary
als.annuse only. fauunxgilii,ayryearsotlse,sainndthbeacgtearridaenmsa,ypabrealcleolnintagmtihneanhtyp“owteheedsisz”eodrromleasyopflatyheadaudxitiiloianrayl
nu
ournal bacteriaandyeastsinattinegardens(seeabove).
arjso
m er
ded fro5. For p 3.EVOLUTIONARYORIGINSOFINSECTAGRICULTURE
a0
nlo14/
w1/ Phylogenetic analyses reveal nine independent origins of insect agriculture
o1
63-595. DAustin on (ifnFunitghgueicrAeul2mt;uaTrzeaoblnilkerea2wi)n.isfIoenrhaenasdtts(a,Mfsuiunnegglalleelrcoeurtilgtaiivln.a,2tai0op0np1ra;orSoxcsimheuoalnttezlyl&yo2nM4c–ee3,iep4rrMo1b9ya9ab5il)ny.I4thn5e–teA6r5mfrMiicteyasna,
005.36:5Texas - rbaeientfloerse,shto(wAeavneern,aegtraicl.u2lt0u0re2;arDo.sKe.inAdaenpeennd&enPt.lyEgsegvleetnotnim,seusbbmeittwteede)n.2In0–a6m0bMroysiaa,
st. 2y of sixtimesinvariousnonxyleborinelineages,andonceintheancestoroftheXyle-
Sysit boriniabout30–40Mya(Farrelletal.2001).Whereasthecommonancestorsof
ol. ver the macrotermitines and of the xyleborines each domesticated a single, specific
EvUni primarycultivarcladetowhichtheirdescendantshaveadheredthroughoutsubse-
col. by quentevolution(Figure2,Table2),attineantsmaintainassociationswithmultiple
E
v. independently domesticated cultivar lineages (which are for the most part very
e
u. R closelyrelated;Muelleretal.1998;Munkacsietal.2004;Table2).Interestingly,
nn therearenoknowncasesofreversalfromagriculturaltononagriculturallifeinany
A
ofthenineagriculturalinsectlineages(Figure2a,2b,and2c),suggestingthatthe
transitiontofungicultureisadrasticandpossiblyirreversiblechangethatgreatly
constrainssubsequentevolution.
Twomainmodelshavebeensuggestedfortheindependentevolutionarytran-
sitionstoagricultureininsects,the“consumption-first”versusthe“transmission-
first” models (Mueller et al. 2001). In the consumption-first model (the likely
modelforthetermites),aninsectlineageinitiallybeginstoincorporatefungiinto
itsmoregeneralistdiet,thenbecomesaspecializedfungivore,andfinallyevolves
adaptationsforcultivatingfungi.Inthetransmission-firstmodel(thelikelymodel
forthebeetles),theinsectlineagebeginsitsassociationwithafungusbyserving
20Oct2005 12:41 AR ANRV259-ES36-24.tex XMLPublishSM(2004/02/24) P1:OJO
570 MUELLERETAL.
Humans Multipleindependentoriginsofagriculture 10,000yearsagofortheearliestknownoriginsofhumanagriculture;multipleregionsoforigin Multiplecropcladesfromdiverselineagesofplantsandfungi
g
Annu. Rev. Ecol. Evol. Syst. 2005.36:563-595. Downloaded from arjournals.annualreviews.orby University of Texas - Austin on 11/14/05. For personal use only. devolutioninant,termite,beetle,andhumanagriculture Agriculturein: AttineantsMacrotermitinetermitesXyleborineambrosiabeetles SingleoriginofagricultureSingleoriginofagricultureSingleoriginofagricultureinintheAttiniintheMacrotermitinitheXyleboriniNootherantpracticestrueNoothertermitepracticesAgricultureoriginatedagriculture,butsomeantstrueagriculture,buttheindependentlyinsixallowfungitogrowintheirdistantlyrelatedtermiteadditionalambrosiabeetleSphaerotermesnestwallsforstructuralorlineages;theseotherbeetlesphaerothoraxantibioticpurposes.promotessystemsarelesswellthegrowthofbacteriainunderstood(seetext).foodstores. 45–65MyainAmazonian24–34MyainAfrican30–40Myainxyleborinerainforestsrainforestsbeetles;regionoforiginunknown21–60Myaintheothersixambrosiabeetlelineages MultiplecultivarcladesSinglecultivarcladeMultiplecultivarcladesOnecultivarcladebelongsAlltermitecultivarsbelongTheambrosiacultivarsTermitomycesAmbrosiellaRaffaelleatothePterulaceae;atleasttothegenus.andthreeadditionalhaveapolyphyleticoriginpolyphyleticcultivarcladeswithinthegeneraOphiostomabelongtotheLepiotaceaeandCeratocystis(tribeLeucocoprineae)..
n
a
y
g n
TABLE2Cropecolo Cropecology&evolutio Numberofinferredevolutionaryoriginsofagriculturalbehavior Estimateddateandregionoforiginofagriculturalbehavior Numberofcropcladescultivated
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EVOLUTIONOFAGRICULTUREININSECTS 571
Present Notapplicable NotapplicableSpecializationoncropsishistoricallymanifestedbydifferenthumanlineages(reflectingseparatedomesticationevents),butnosinglehumanlineageisnearlyasspecializedonasinglecropasaretheinsectfarmers. Continued()
g
st. 2005.36:563-595. Downloaded from arjournals.annualreviews.ory of Texas - Austin on 11/14/05. For personal use only. VariablePresentVerticalcultivarinheritanceVerticalcultivarinheritanceisistypicalfortwotheruleinallxyleborineindependentlyderivedlineages.macrotermitelineages;allothermacrotermitinesacquirecultivarshorizontallyviawind-dispersedsporesfromothercolonies. Clade-cladecorrespondenceNostrictclade-cladeDefinedcladesoftermitecorrespondencespeciesarespecializedinThefungallineagesthattheyonlygrowfungiassociatedwithxyleborinetypicalfortheirownambrosiabeetlesareonlytermite-specificcultivardistantlyrelatedtoeachclade.other,andallarealsoassociatedwithsomebarkbeetles. PresentPresentSingletermitespeciesSinglebeetlespeciesgenerallyassociatewithgenerallyassociatewithmultiplefungallineages,multiple,distantlyrelatedbutwithinthelimitsoffungallineages;theprimaryspecificcultivarclades(seecultivaristypicallyasingleabove);however,somefungalspecies,buttermitespeciesareverysecondarycultivarsvaryandspecializedonaparticularoftencomefromdifferentfungus.fungallineagesthantheprimary-cultivarlineage.
Annu. Rev. Ecol. Evol. Syby Universit PresentVerticalcultivarinheritanceistheruleinallattineantlineages. Clade-cladecorrespondenceDefinedcladesofantspeciesarespecializedinthattheyonlygrowfungitypicalfortheirownant-specificcultivarclade. PresentInallcasesstudiedindetail,singlespeciesofantsgrowonlyasingle,phylogeneticallynarrowgroupoffungi(i.e.,asingle,phylogeneticallydefined“species”offungus).
e
c
CroptransmissionVerticalcultivarinheritanfromparenttooffspring(i.e.,cultivartransferbetweengenerations) SpecializationoncropsSpecializationathigherphylogeneticlevels Specializationatleveloffarmerspecies
20Oct2005 12:41 AR ANRV259-ES36-24.tex XMLPublishSM(2004/02/24) P1:OJO
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Humans PresentLateralexchangeofcultivarsbetweenfarmersocietiesisaprominentfeatureofhumanagriculture. Notapplicable AbsentSometraditionalcultivationregimes(e.g.,potatofarminginthe
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st. 2005.36:563-595. Downloaded from arjournals.annualreviews.ory of Texas - Austin on 11/14/05. For personal use only. Agriculturein: MacrotermitinetermitesXyleborineambrosiabeetles UnknownUnknownLateralcultivarexchangeisprobablyrare,butmayoccurwhengalleriescontainingbroodoftwoormorefoundressfemales,eachcarryingadifferentcultivar(e.g.,differentspeciesoffungi),occurincloseproximityinthesametree. PresentRareHorizontalcultivarexchangeHorizontalcultivarexchange(throughwind-dispersedoccursatleastoccasionally.spores)istypicalformosttermitelineages. AbsentAbsentWildpopulationsareWildpopulationsareunknownfortermiteunknownforambrosiacultivars.beetlecultivars.
Annu. Rev. Ecol. Evol. Syby Universit Attineants PresentWithinaspeciesofant,cultivarsareprobablyoccasionallyexchangedbetweencolonies(e.g.,aftercultivarlosswhencultivar-deprivedcoloniesmayacquirereplacementcultivarsfromneighboringcolonies). PresentHorizontalcultivarexchangeoccursbetweensympatricantspeciesiftheyarespecializedonthesamecultivarlineage. VariablePrimitiveattineantsprobablyimportnovelcultivargenotypes
Table2Continued() Cropecology&evolution CropsharingandcropexchangeLateralexchangeofcultivarswithinthesamefarmerspecies(i.e.,exchangewithinsamefarmergeneration) Cultivarexchangebetweenfarmerspecies Geneticexchangebetweendomesticatedandwildpopulations(e.g.,geneticinterbreedingbetween