C H A P T E R 1

TheSignificanceofSymbiosis

Individuals of different species form persistent associations fromwhichtheyallbenefit.Theserelationshipsaresymbioses.Thecorepur­poseof thisbookis toassessthebiologicalsignificanceofsymbiosesandto investigatetheprocessesbywhichsymbiosesareformedandpersistinbothevolutionaryandecologicaltime.Symbiosesarebiologi­cally importantbecausetheyarewidespreadanddominatethebiotaof many habitats. I address this aspect of the biological significanceof symbiosis later in thischapter.For thepresent, I suggest thatanydoubtingreadersshould“lookoutofthewindow”andlisteveryor­ganismtheycansee.Icanguaranteethatmost,probablyall,organismsonthelistareaproductofsymbiosis.Theprevalenceofsymbiosesisnot,however,theonlyreasonwhysymbiosesshouldbeimportanttobiologists.Anadditionalreasonisthatsymbiosischallengestwowidelyacceptedtenetsofbiology:theuniversalityofdescentwithmodifica­tioninevolution,andtheprimacyofantagonismininteractionsamongorganisms.Iwillstartbyexplainingthesechallenges.

1.1 Symbiosis as a Source of Novel Traits

The core expectations of evolution by descent with modification arethatmorphological,physiological,andothertraitsofanorganismarederivedfromtraitsintheancestorsoftheorganism,andthatchangesinthesetraitscanbedescribedbymultiple,smallstepswitheachinter­mediateconditionviable.Mosttraitscanbeexplainedinthisway,butthereisunambiguousevidencethatsometraitsofgreatevolutionaryandecological importancehavebeengained laterally fromdifferent,oftenphylogeneticallydistant,taxa.Somelaterallyacquiredtraitsarenovelfortherecipientorganismandtheycanbeevolutionaryinnova­tions, i.e.,“newlyacquiredstructuresorpropertieswhichpermit theassumptionofanewfunction”(Mayr1960,p.351)].

Thereare two routes for the lateralacquisitionof traits: symbiosisandhorizontalgene transfer.Entireorganismsareacquiredbysym­biosisandso the traitsgainedcanbegenetically,biochemically,andeven behaviorally more complex than those obtained by horizontal

� • Chapter1

transferofisolatedgenes.Twoverydifferenttypesofsymbiosisillus­trate thispoint.Theeukaryoticcells thatacquired thecyanobacterialancestor of plastids gained the capacity for oxygenic photosynthesisas a single package, including many correctly expressed genes, theintegratedmolecularandcellularmachineryfortheassemblyofmulti­component photosystems in photosynthetic membranes, and the en­zymaticmachineryforcarbonfixation.Similarly,anAcaciatreethatisprotectedfromherbivoresbyaresidentcolonyofantshasacquiredamorphologicallyandbehaviorallycomplexdefensecapableofrespond­ingappropriatelytoherbivoreattacksofvariablemagnitudeandtype.

The appreciation that descent with modification is an inadequateevolutionaryexplanationdoesnotmeanthatsymbiosescontradictcur­rentunderstandingofevolutionaryprocesses.Symbiosesaresubjecttonaturalselectionand,contrarytosomeclaims(e.g.,Ryan�003), theyhavenodiscernibledynamicindependentofnaturalselection.

1.� Symbiosis as a Type of Biological Alliance

Interactions among organisms are routinely portrayed as principallyantagonistic, dominated by competition, predation, and parasitism.Thehistoryoflifehasevenbeendescribedas“afourbillionyearwar”(Marjerusetal.1996).Thisperspective isnotwrong,but it is incom­plete.Organismshaverepeatedlyrespondedtoantagonists(predators,competitors,etc.)andabioticstressessuchaslownutrientavailabilitybyformingalliances,i.e.,interactionswithotherorganisms,resultinginenhancedfitnessandecologicalsuccessofalltheparticipants.Aswithalliancesamongpeople,politicalparties,andnationstates,thepersis­tenceofmanybiologicalalliancesdependsonthecontinuedpresenceoftheantagonist,andthebenefitgainedfromthealliancecanvarywiththeidentityoftheparticipantsandenvironmentalconditions.Ireturntothisissueinsection1.3.

Mostalliancesarefoundedonreciprocity,thatitisadvantageoustohelpanotherorganismonlyifthefavorisreturned.Inatwo­organismsystem,reciprocityrequiresthateachoftheorganismsplacesahighervalueonwhatitreceives(benefit)thanwhatitgives(cost)(figure1­1a).For example, the relationship between mycorrhizal fungi and plantroots is underpinned by the transfer of photosynthetic sugars fromplant tofungus,andofphosphate inthereversedirection.Photosyn­thetic carbon is cheap for theplant toproducebuta critical resourcefor the fungus, which cannot utilize the polymeric carbon sources insoil.Inorganicphosphateisrelativelyimmobileinsoils,andisacquiredmorereadilybythefine,branchingfungalhyphaethanbytherelatively

3TheSignificanceofSymbiosis •

(a)-10 +30

+30 -10

Manyorganismsinalliancesdisplaycooperativetraits,i.e.,traitsthatare advantageous to another organism (the recipient) and that haveevolvedbecauseof theirbeneficialeffecton therecipient.TheAcaciatrees introduced in section 1.1 display cooperative traits that bene­fittheirresidentants:swollen,hollowthornswhichprovidedomatia(nestsites)fortheants,andextrafloralnectarandhighlynutritiousant­bodiesonwhichtheantsfeed(figure1­�).Inreturn,variousbehavioral

massiveplantrootswithshort,nonbranchingroothairs.Theonesitu­ationwherereciprocityasdepictedinfigure1­1adoesnotapplyisbe­tweencloselyrelatedorganisms.Here,kinselectionisimportant:geno­typesthathelprelatives(i.e.,individualswithmanygenesincommon)increaseinfrequencyandareataselectiveadvantageovergenotypes

TR

AIT

Biologicalalliances.(a)Mostalliancesareunderpinnedbyreciproc­itybetweenthetwoparticipatingorganisms,XandY. Eachorganismprovidesaserviceatcostof10arbitraryunitsandreceivesabenefitof30units,yield­ingnetbenefitof�0units. (b)Alliancesareclassifiedaccording to thenum­berof speciesand traits involved.Examplesofeach typeofalliance include(A)roostingbatshuddlingtogether,sharingtheiruniformtraitofheatproduc­tion; (B) mixed­species flocks of passerine birds foraging for food in winter;(C)barteringofgoodsbetweenhumans;and(D)consortiaofmultiplemicro­bialspeciesthat,throughtheircomplementarymetaboliccapabilities,degradeotherwiserecalcitrantorganiccompounds.[Figure1­1amodifiedfromfigure1

net +20 +20

NUMBER OF SPECIES (b)

One >One

A B

DC

Figure1­1

ofDouglas(�008)]

thatdonothelp.

� • Chapter1

Figure1­� AdaptationsofAcaciasphaerocephalaforsymbiosiswithprotectiveantsofthegenusPseudomyrmex.(a)Hollowthornsthatprovidedomatia(nestsites)forants.(b)Extrafloralnectaryatbaseofleaf.(c)Lipid­richant­bodyattipof leaflet. [Reproduced fromfigure�­18ofE.O.Wilson (1971)The InsectSocieties.HarvardUniversityPress]

traitsoftheantsareadvantageoustotheplant,includingpatrolingtheplanttoprotectagainstherbivoresandremovingfungalsporesatthebreakpointof theant­bodies toprevent fungal infectionof theplant.Asacontraryexample,thefoodinthegutofananimalinfectedbyatapeworm isnotacooperative traitbecause,although the tapewormbenefitsfromthefood,animalshavenotevolvedthehabitofeatingforthebenefitoftapeworms.

Alliancescanbeclassifiedaccordingtowhethertheyinvolveoneormultiplespeciesdisplayingthesameordifferenttraits,andthistwo­wayclassificationgeneratesfourcategories(figure1­1b).ThefocusofthisbookiscategoryDinfigure1­1b,alliancesbetweendifferentspe­cieswithdifferenttraits.Thesealliancesarealsoknownasmutualisms,whichareformallydefinedasrelationshipsfromwhichallparticipantsderivebenefit.Inthisbook,Iconsidersymbiosesasatypeofmutual­ism,specificallymutualismsinwhichtheparticipantsareinpersistentcontact.

Thisbringsmetothemostfrustratingdifficultyinthefieldofsym­biosis—the lack of a single universally accepted definition. Disagree­mentoverdefinitionshasledtodisputesaboutwhichrelationshipsaresymbioses and, consequently, a lack of consensus about the commonfeaturesofsymbioticsystems.Twoalternativedefinitionsofsymbiosis,neither fully satisfactory, havedominated the literature formany de­cades:“symbiosisasanyassociation”and“symbiosisasapersistentmu­

5TheSignificanceofSymbiosis •

tualism.”Here,Idigressbrieflyfromthecoretopicofthischapter,thesignificanceofsymbioses,toaddressthethornyproblemofdefinitions.

1.3 Definitions of Symbiosis

1.3.1 SymbiosisAsAnyAssociation

ThetermsymbiosiswascoinedoriginallybyAntondeBaryin1879tomeanany association between different species,withtheimplicationthat the organisms are in persistent contact but that the relationshipneednotbeadvantageoustoalltheparticipants.DeBaryexplicitlyin­cludedpathogenicandparasiticassociationsasexamplesof symbio­ses.Manysymbiosisresearchersusethisdefinitionand,withoutdoubt,somecolleaguessteepedinthesymbiosisliteraturewillhaveobjectedtotheopeningtwosentencesofthisbook.

OnekeyadvantageofthedefinitionofdeBaryisthatitpromotesabroadcontextforresearchintosymbioses.Itactsasareminderthatitisimportanttoinvestigateboththecostsandthebenefitstoanorganismofenteringintoasymbiosis(seefigure1­1a);anditisreasonabletoex­pectsomeoftheprocessesunderlyingrelationshipsthatareclassifiedasmutualisticandantagonistictobesimilar.Forexample,justasthepersistenceofcertainantagonisticinteractionsdependsononeorgan­ismfailingtorecognizetheantagonistasaforeignorganism,sosomeorganismsmaybeacceptedintosymbiosesbecausetheyfailtotriggerthedefensesystemsoftheirpartnerandnotbecausetheyarepositivelyrecognizedasmutualists.

Nevertheless, thedefinitionofdeBaryhas twoseriousshortcom­ings.Firstandveryimportantly,thedefinitionisnotacceptedbymostgeneralbiologistsornonbiologiststoday,andsofailstocommunicateeffectively.MostpeopledonotdescribethecurrentmalariapandemicorthepotatoblightthatcausedtheIrishfamineofthe18�0sasexam­plesofsymbiosis.Second,therearefewprinciplesgenerallyapplicabletosymbioses,asdefinedbydeBary,butinapplicabletootherbiologicalsystems.Asa result, the“symbiosisasanyassociation”definition issomethingofacatch­all category.Although thisdefinitiondoespro­motefurtherenquiryandinsightintosymbioses,anyinsightsobtainedareunlikelytobecommontoallsymbiosesdefinedinthisway.

1.3.2 SymbiosisAsaPersistentMutualism

The definition of symbiosis widely accepted among both general bi­ologistsandthelexicographerswhoprepareEnglishdictionariesisan association between different species from which all participating

6 • Chapter1

organisms benefit.Isubscribetothisdefinitioneventhoughitisnotwithoutdifficulties.

The“symbiosisasapersistentmutualism”definitionrequiresaformalassessmentofthebenefitderivedbytheorganismsintheassociation.Thestandardapproachtoidentifybenefitistocompareanorganism’sperformance(survival,growth,reproductiveoutput,etc.) inthepres­enceandabsenceof itspartner. If theorganismperformsbetterwiththepartner,itbenefitsfromtherelationshipandifitperformsbetterinisolation, then it isharmedby theassociation.Althoughthemethod­ologyappearsstraightforward,itisunsuitableformanyassociations.

Thereare two typesofproblem.First, for someassociations, thereareformidablepracticaldifficulties.Considerthedeep­seasymbioses,such as the chemosynthetic bacteria in the tissues of pogonophoranwormsathydrothermalventsandtheluminescentbacteriainthelureofdeep­seaanglerfish.Itisdifficulttoenvisagehowbacteria­freepo­gonophoransandanglerfishcouldbegeneratedexperimentallyandhowtheperformanceof thebacteria­free individualscouldbemoni­toredreliablyinhabitatssoinaccessibletohumans.

Thesecondandmorefundamentalproblemisthevariabilityofrealassociations,suchthatbenefitisnotafixedtraitofsomerelationshipsbutvaries,especiallywithenvironmentalcircumstance.Toillustratethisissue,letusconsiderhermitcrabsofthegenusPagurus.Hermitcrabsliveinemptyshellsofgastropodsthatareoftencolonizedbybenthiccnidarians,suchasseaanemonesandhydroids.Generally,thecnidar­ianbenefitsfromsettlingontoashellinhabitedbyahermitcrabbecauseithasreadyaccesstoscrapsoffoodproducedwhenthecrabeatsandbecause the mobility of the crab in its shell introduces the cnidariantodifferenthabitatsthatmayincreasefoodavailabilityandreducetheriskofburialinsediment.Thehermitcrabiswidelybelievedtobenefitbecausethecnidariancanactasabodyguard,protectingitfrompreda­torsbyfiringdeterrentandoftentoxicnematocystsfromitstentacles.Forexample,theseaanemoneCalliactisparasiticaeffectivelydetersoc­topuspredationofPagurusspecies(Ross1971).Theprotectivevalueofhydroidsis,however,variable.Predationratesofhermitcrabscanbeelevatedordepressedbyhydroids,dependingonthepredatorspecies,andtheunderlyingfactorsarecomplex.Forexample,BuckleyandEber­sole(199�)investigatedPaguruslongicarpusinhabitingshellscolonizedbythehydroidHydractiniaspp.andsubjecttoattackbythebluecrabCallinectessapidus.Inaquariumtrials,hermitcrabsinshellsbearinghy­droidsweresignificantlymorelikelythanthoseinhydroid­freeshellstobeeatenbybluecrabs(figure1­3a).Thedifferencearosebecauseittooklongerforthebluecrabstocrushthehydroid­freeshells,oftengiv­ingtheresidenthermitcrabtimetoescape.FurtheranalysisofBuckley

7TheSignificanceofSymbiosis •

Figure 1­3 Impact of the association with hydroids on the susceptibility ofthehermitcrabPaguruslongicarpustopredationbyCallinectessapidus.(a)Oc­cupation of hydroid­bearing shells significantly depressed the frequency ofP.longicarpusthatescapedfromC.sapidusattack(c� =6.158,p<0.05).(b)Me­chanical strength of shells inhabited by P. longicarpus, either colonized byhydroids(opensymbols)orlackinghydroids(closedsymbols).[RedrawnfromdatainBuckleyandEbersole(199�)]

andEbersole(199�)revealedthatshellsbearingthehydroidsweremorelikelythanhydroid­freeshellstobecolonizedbyburrowingpolychaeteworms(Polydoraspecies),andthetunnelsofthesewormssignificantlydepressedthemechanicalstrengthoftheshells(figure1­3b).

Thiscomplexmultiwayinteractionbetweenhermitcrabs,hydroids,burrowing polychaete worms, and the predatory blue crabs raises a

8 • Chapter1

question:whydothehermitcrabseveruseshellsbearingthehydroids?One possible explanation is that the hydroids may protect the shellfromcolonizationbylargesessileanimals,suchasslipperlimpetsorbivalves,whichwouldmaketheshellveryheavyandunbalancedforthehermitcrab.Basedontheseconsiderations,dohermitcrabsbenefitfromassociatingwithhydroids?Theansweristhat“italldepends”—ontheincidenceofburrowingworms,theidentityandabundanceofpredators,andtheincidenceofsettlinglimpets.Allofthesefactorsareanticipatedtovarywithsiteandseason.

Asthehermitcrabassociationillustrates,manyrealassociationsarecomplexandvariable.Thisdoesnotunderminethedefinitionofsym­biosisasamutuallybeneficialassociation,providedthedefinitionre­ferstotheinteractionbetweentheorganisms,nottheorganismsthem­selves.Anorganismthatentersintoamutuallybeneficialrelationshipissymbioticinthecontextofthatrelationship;butif,throughachangein environmental circumstance or other factors, the relationship be­comesantagonistic, then it isno longera symbiosis. In thisway,as­sociationswithvariableoutcomesfortheparticipatingorganismsaretransformedfromaproblemforthedefinitionofsymbiosistoanop­portunitytoexplorethefactors thataffect the incidenceofsymbiotic(i.e.,mutuallybeneficial)interactions.

Thefluidityof somebiological interactions isparticularlyapparentforsomeorganismsthatwereoriginallyidentifiedasparasitesbutarenowrealized tobeharmlessorevenadvantageous topartnersundercertain circumstances. For example, the fungus Colletotrichum magnawasfirstidentifiedasavirulentpathogenofcertainplantspecies(fig­ure1­�a)butitsimpactonplantgrowthwassubsequentlyfoundtode­pendontheplantspeciesandevencultivar,suchthatthefungalinfec­tionpromotesthegrowthofsomeplants(figure1­�b)andcanprovideprotectionfromdroughtorpathogens(Redmanetal.�001).Similarly,thebacteriumHelicobacterpylori inthehumanstomachisbestknownasthecauseofulcersandgastriccancerinadults,especiallyolderpeo­ple,but inchildrenandyoungpeople,H.pylori isharmlessandmayevenbebeneficial,providingprotectionagainstdiarrhoeaandasthma(BlaserandAtherton�00�).Inthesameway,organismswhichareusu­allyharmlessorbeneficialcanbedeleterioustotheirpartnersundercer­taincircumstances.ThetinymiteDemodexfolliculorum,<0.5mmlong,isacommensalofhumans.Itlivesexclusivelyinhairfollicles,includingtherootsofeyelashes,andreproducessexuallywithagenerationtimeof�–3weeks.Itoccursinmostadultsandmanychildren,anditisgener­allyharmless.Occasionally,however,theinfectionsareheavyanddel­eterious,causingitchingandswelling.Similarly,thearbuscularmycor­rhizalfungiareusuallybeneficialsymbiontsofplantrootsbuttheycan,

9TheSignificanceofSymbiosis •

Figure1­� Impactof the fungusColletotrichummagna (strainL�.5)onplantgrowth:(a)pathogeniconcucumber;(b)beneficialandapparentlyneutralfortwotomatocultivars.s.e.indicatesstandarderror.[DrawnfromdatainRed­manetal.(�001)]

occasionally,beharmfultotheplants.Forexample,Glomusmacrocarpumcausesastuntingdiseaseoftobaccoplants(ModjoandHendrix1986).

Ifavorthedefinitionofsymbiosisasapersistentmutualismbecauseits scope provides a meaningful biological framework for one of thekeyquestionsexploredinthisbook:Howdomutuallybeneficialinter­actionsbetweendifferentspeciesevolveandpersist?

1.3.3 DurationofContact

Forhowlongshouldthepartnersinaninteractionbeincontactfortherelationshiptobecalledasymbiosis?Itiswidely,butnotunanimously,acceptedthattheansweris:atleastasubstantialproportionofthelife­spanoftheinteractingorganisms.Ithasonlyrarelybeenarguedthatthepredationofgazellesbylions,therapiddeathofpeopleinfectedbytheEbolavirus,andthepollinationofplantsbyfleetingvisitationsofforagingbutterfliesaresymbioses(e.g.,Lewis1985).

Some examples bring into focus the problem posed by the defini­tionofsymbiosisasapersistentassociation.Letusconsiderfirst therelationshipbetweenhumansandhoneyguidebirds,twospeciesthatsharea taste forhoney.Thebirdcannotaccess thehoney frommostbeecolonies,butappearstohaveabetterknowledgethanpeopleofthelocationof thecolonies. Intheirstudyof theBoranpeople inKenya,IsackandReyer(1989)foundthatthehoneyguideleadspeopletobeenestsbycallingandflyingshortdistanceseverclosertothenest,and

10 • Chapter1

thenchangesitscallandflightpatternintheimmediatevicinityofthenest.Thepeopleopenupthenesttoharvestthehoney,andthebirdfeedsonthehoneycombfragmentsthataretoosmallforthepeopletoharvest.Theparticipantsinthisrelationshipdonotmakecontactandsotherelationshipisnotasymbiosis.

At the other extreme of persistence are the vertically transmittedmicroorganisms in some animals, where contact persists beyond thelifespanofanindividualhost.Thecomplementofintracellularbacteriainsomeinsectsisacquiredexclusivelyfromthemotherinsect,usuallybytransferfromthecellshousingthebacteriatotheovariesandinser­tionintotheunfertilizedegg.Obligateverticaltransmissioncanresultinassociationspersistingcontinuouslyoverlongevolutionarytimescales.Asanexample,thereisgoodphylogeneticevidencethatthebacteriumBuchneraaphidicola, thevertically transmittedsymbiontofaphids,haspersistedthroughgenerationsofitsinsecthostsforatleast160millionyears(Moranetal.1993);andthemitochondriahavebeentransmittedverticallyforupto�000millionyears(EmbleyandMartin�006).

Thedifficultiesforadefinitionofsymbiosisasapersistentassociationariseforrelationshipswithanintermediatedurationofcontact.Thisisillustratedbyinsectpollinationofplants.Formanyplants,contactwiththepollinatorisbrief,aslittleasafewseconds,whiletheinsectcollectsnectarorpollen.Asalreadyconsidered,theseinteractionsarenotusu­allydeemedtobesymbioses.Amongorchids,however,thedurationofcontactmaybeprolongedtominutestohours,oftenwithelaboratemechanismstoensurepollentransfertoaspecificlocationontheinsect.Thisconditionrelatestothefactthatthepollengrainsoforchidsarenotseparate but held in compact structures called pollinia, such that anorchidflower isdependentona single insect forpollen transfer.AnexceptionalexampleistheorchidCoryanthes.AsBarth(1991)describes,thecomplexCoryanthesflowers(figure1­5)traptheirpollinatingbees,Eulaema,forlongperiods.Thenarrowbaseoftheflowerlipexudesaliquidscent,which thebeecollectsbyscratchingwith its forelegs. Itoftenslipsoffthelip,intothebucketbelow.Thebucketcontainsawa­terysolution,exudedfromthecolumnoftheflower,andthebeeswimsaboutinthewater.Theonlyexitisviaanarrowholeattheapexofthelip,anditmaytakethebeehalfanhourormoretoescape.Ifthebeeiscarryingpolliniafromanotherflower,thepolliniaaretransferredtothestigma;andthepolliniafromthecurrentfloweraretransferredtotheabdomenofthefirstbeetotakethisroutethroughtheflower.Evenmorepersistentplant­pollinatorcontactisdisplayedbytheplantswithbrood­sitepollination,includingthefigs(Ficus)pollinatedbyagaonidwaspsandYuccaspeciespollinatedbymoths. In these systems (dis­cussedfurtherinchapter3,section3.�.�),pollinationislinkedtoinsect

TheSignificanceofSymbiosis • 11

Figure1­5 TheflowerofCoryanthesorchid.Arrowsshowthecourseofthepol­linatinginsect.Seetextfordetails.[Redrawnfromfigure7.�7ofBarth(1991)]

deposition of an egg into some of the flower ovules. Seed set in theovulesbearinginsecteggsisabortedandtheinsectoffspringdevelops,toadulthoodforthepollinatorsofFicusandthroughlarvaldevelop­mentfortheYuccapollinators(whichpupateinthesoil).

Asimilarcontinuuminthedurationofcontactisdisplayedbythemicrobiotainanimalguts.Membersofthegutmicrobiotavarygreatlyintheirpersistence,fromtransients,enteringandleavingthegutwiththefood,toresidents,retainedformuchoftheanimallifespan.AclassicillustrationisthestudyofEscherichiacoliserotypesinasinglehumanvolunteerover11months.Ofthe53typesidentified,mostpersistedforonetoafewdaysandjusttwotypespersistedforthefulldurationoftheexperiment(Caugantetal.1981).

AmongtheE.colitypesthatvaryintheirpersistenceinthegutsofhumansandamongthevariouspollinationsystemsdescribedabove,thereisnominimalresidencetimethatcanbeusedmeaningfullyasacriterionforsymbiosis.Inotherwords,itisbiologicallyunrealistictocreateasimpledichotomybasedondurationofcontactbetweenrela­tionshipsthatare,andarenot,symbioses.Theseissueshaveabearingontheframeworkfor thisbook.AlthoughIwillconformtothecon­ventionthatrelationshipswithnoorfleetingphysicalcontactarenotsymbioses,Iwillusetheserelationshipsasexamplestoillustrateanddevelopideasthatarerelevanttosymbioses.

1� • Chapter1

Letusnowreturnfromthedigression intodefinitionsto themainpurposeofthischapter:thesignificanceofsymbiosis.Inthefollowingsection,Iprovideabriefprimerontheevolutionaryandecologicalsig­nificanceofsomesymbioses.

1.� The Biological Significance of Symbioses

1.4.1 MisunderstandingsabouttheSignificanceofSymbioses

The biological importance of symbioses is central to current under­standingoftheserelationships.Thisopeningsentencecouldnothavebeenwrittenthroughoutthegreaterpartofthetwentiethcentury,whenmutuallybeneficialsymbiosesweretreatedascuriositiesofnaturethatwere ecologically unstable and evolutionarily transient (Sapp 199�).Theecologicalargumentfortheinstabilityofsymbioseswasthat,byLotka­Volterraequations,mutuallybeneficialinteractionsleadtoun­controlledpopulationincreasewhileantagonisticinteractionstendtostabilizepopulations(figure1­6).Theevolutionaryargumentwasthatgenotypeswhichconferbenefitonnon­kinareataselectivedisadvan­tage relative to selfish genotypes which provide no benefit. The im­plicationisthatsymbiosesfailinecologicaltimebecausetheyaretoomutualisticandinevolutionarytimebecauseoftheselectionpressuretobelessmutualistic.Bothperspectivescannotberightand,inreality,botharewrong.Thereasoningunderlyingeachperspectiveisbasedontheerroneousassumptionthatsymbiosesareperfectlymutualistic.Inreality,thepartnersinsymbiosesareofteninconflict,buttheconflictismanagedandcontrolled.Theseissuesareexploredinchapter3.Here,Iconsiderthebiologicalsignificanceofsymbiosesinthreerespects:asasourceofnovelcapabilities,intheevolutionofeukaryotes,andasadeterminantoftheecologicalsuccessofsomeplantsandanimals.

1.4.2 SymbiosisAsaSourceofNovelCapabilities

Formanysymbioses,oneorganismprovidesabenefitthatisdifferentfromanypreexistingtraitinitspartner.Asconsideredinsection1.1,suchabenefitcanbeanevolutionaryinnovation.Thenovelcapabilitiesgainedinthiswayareverydiversebutmanycanbeclassifiedasoneoffourfunctions:accesstoanovelmetaboliccapability,protectionfromantagonists(predators,pathogens,etc.),mobility(includingdispersal),andagriculture.Table1­1providessomeexamplesofsymbiosesandothermutualismsaccordingtothesefunctions.

Forsymbiosesthatinvolvereciprocalexchangeofservices,thebene­fitsgainedbythedifferentpartnerscanbefunctionallydistinctorvary

TheSignificanceofSymbiosis • 13

Figure 1­6 Projected population size of interacting organisms in (a) an an­tagonisticinteractionsuchasapredator­preyrelationshipand(b)interactionbetweenpopulationsoftwomutualists,herelabeledas1and�.

with circumstance. The Acacia­ant symbiosis illustrated in figure 1­�involvesthereciprocalexchangeoffoodforprotectionasprovidedbytheplantandants,respectively.Asconsideredearlier inthischapter(section1.�),themycorrhizalsymbiosisbetweenplantrootsandfungiisprimarilynutritionalundermostenvironmentalconditions,withtheplantgainingmineralnutrientsfromthefungus,andthefungusgain­ingphotosyntheticsugarsfromtheplant;buttheinteractionsarenotuniform. For example, the principal advantage of this symbiosis fornaturalpopulationsoftheplantVulpiaciliataisprotectionfromfungalpathogens(Newshametal.1995).

Animalbehavioriscentraltothecapabilitiesacquiredbysomesym­bioticorganisms.Thisappliesparticularlytoanimal­mediateddisper­sal,agriculture,andsomeinstancesofprotectionfrompredators(seetable1­1).Agricultureisofparticularinterestinthiscontext.Agricul­turecanbedefinedasthecultivationofadifferentspeciesandthecon­sumptionofaproportionofthatorganismoritsproducts.Itinvolvesinoculatingasuitablesubstratumwiththecultivatedorganism,whichis then tended toensure itsgrowthandprotection fromcompetitorsandpathogens.Linkedtothecomplexbehaviorrequired,farminghasaveryrestricteddistribution,largelylimitedtohumans,ants,termites,andbeetles.Fungiarefarmedbyattineants,termitesofthesubfamilyMacrotermitinae,andvariousbeetles, including theambrosiabeetles(PlatypodinaeandsomeScolytinae)(Wildingetal.1989;Farrelletal.�001).Somesymbiosesbetweenantsandhemipteraninsectsalsohavethetraitsofagriculture,withthehemipteransfarmedbyantsfortheirhoneydew(seechapter5,section5.�.1).

Table 1­1Survey of Benefits Gained from Symbioses and Nonpersistent Mutualisms

Relationship Examples

(a)Accesstometaboliccapability

Inorganiccarbonfixation Cyanobacteria­derivedplastidsinalgaeandplants

Algae/cyanobacteriainlichenizedfungi,protists,andanimals

Mycorrhizalandendophyticfungiassociatedwithplants

Chemosyntheticbacteriainanimals

Aerobicrespiration Bacteria­derivedmitochondriaineukaryotes

Nitrogenfixation Bacteria(e.g.,rhizobia,Frankia,cyanobacteria)inplants

CyanobacteriainlichenizedfungiBacteriainafewinsects(e.g.,termites)

Cellulosedegradation BacteriainvertebratesProtistsinafewinsects(e.g.,“lower”

termites,woodroaches)FungiinMacrotermitidae

Nutrientbiosynthesis(e.g.,vitamins,essentialaminoacids)

Bacteriaorfungiinanimals,especiallyinsects,andinprotists

Degradationoftoxins Bacteriainanimalguts

Toxinproduction Bacteriainanimals(e.g.,insects,bryozoans,sponges)

Fungiinplants

Hydrogenconsumption Methanogenicbacteriainanaerobicprotists

Luminescence Bacteriainsomefishandsquid

(b)Protectionfromantagonists

Protectionfromherbivores Antsassociatedwithplantsremoveordeterherbivores

Protectionfrompredators Antsdeterpredators/parasitoidsofhemipteraninsectsandlycaenids

Seaanemone/hydroidsprotecthermitcrabs

Removalofectoparasites Fromclientfishbycleanerfish;fromungulates(e.g.,gazelle)bypeckingbirds

Protectionfrompathogens Microbiotainanimalgutsandplantrhizosphere(immediateenvironsofroots)

TheSignificanceofSymbiosis • 15

Table 1­1(cont.)

Relationship Examples

(c)Dispersal/mobility

Bioticpollination Malegamete(pollen)transportedtostigmaofplantsbyinsects,birds,mammals

Bioticseeddispersal1 Seedstransportedawayfromparentplantbybirds,mammals,ants

Ant­tendedhemipterans Transporttosuitablefeedingsitesonhostplants

(d)Agriculture� Cultivationoffungibybarkandambro­siabeetles,termites,andattinineants

Cultivationofhemipteraninsectsbysomeants

1 Thiscategoryreferstoseeddispersalbyanimalsthatforagefor(a)seedsbutfailtoeatthemallor(b)plantproductsassociatedwithseeds,e.g.,fruitsconsumedbyvariousbirds and mammals, elaiosomes (lipid­rich structures) consumed by ants. Seeds thatbecomeattachedtothesurfaceofanimals(e.g.,hookedseedsonthefurofmammals)areexcludedbecausetheinteractionispassiveandfunctionallycomparabletowinddisper­sal(Herrera�00�).

�Defined as the cultivation of another organism and consumption of the cultivatedorganismoritsproducts.

Inmanysymbioses,thecontrastingtraitsoftheparticipatingorgan­isms are underpinned by a difference in their metabolic capabilities.Thecapabilitiesarecomplementary,withtwoormoreorganismscon­tributingdifferentelementsofacommonmetabolicpathway,resultinginthenetsynthesisordegradationofcertaincompounds.Forexample,bacteriaofthegeneraClavibacterandPseudomonascandegradethetoxicherbicideatrazinetocarbondioxideandammoniawhenculturedto­getherbutnot individually (DeSouzaetal.1998)because theyhavecomplementarymetaboliccapabilities(figure1­7).Thesebacteriacom­priseaconsortium,meaningthattheinteractingbacteriaperformmorecomplexcapabilitiesthaneitherdisplaysonitsown.Inthisparticularsystem, thecollectivecapabilitiesof theconsortiumareenhancedbycross­feedingofmetabolitesbetweenthepartners.

Inothersymbioses, themetaboliccapabilitiesof theorganismsareunequal,withoneorganismgainingaccesstocapabilitiespresentonlyinitspartners.Theseassociationsgenerallyinvolveeukaryotes,which,asagroup,aremetabolicallyimpoverishedrelativetobacteria.Thelin­eagethatgaverisetotheeukaryoteslackedthecapacityforaerobicres­piration,photosynthesis,andnitrogenfixation;manyeukaryotesthat

16 • Chapter1

Figure1­7 Degradationofthes­triazineherbicideatrazinetocarbondioxideandammoniabyaconsortiumofClavibacterspp.andPseudomonasspp.[Repro­ducedfromfigure6ofdeSouzaetal.(1998)withpermissionfromtheAmeri­canSocietyforMicrobiology]

feed holozoically, including all animals, additionally cannot synthe­size9ofthe�0aminoacidsthatmakeupprotein(theessentialaminoacids)andvariouscoenzymesessentialtothefunctionofenzymescen­traltometabolism(vitamins,suchasbiotin);vertebratesadditionallylackthecapacitytodegradethecelluloseandrelatedpolysaccharidesthataccountfor90%ormoreofplantmaterial;andarthropodscannotsynthesizesterols,includingcholesterolwhichisanessentialcompo­nent of eukaryotic membranes. On multiple evolutionary occasions,eukaryoteshaveacquiredthesemetaboliccapabilitiesbyenteringinto

TheSignificanceofSymbiosis • 17

relationshipswithmicroorganisms.Forexample,variousplantsgainaccesstonitrogenfixationbyassociatingwithnitrogen­fixingbacteria;someanimals,suchascorals,andthelichenfungigainphotosynthesisbyassociatingwithalgae;andotheranimalsderivespecificnutrients,includingessentialaminoacidsandBvitamins,fromsymbioticbacte­ria.Theservicesprovidedinthesesymbiosesarenutritional.

Some organisms benefit from symbioses with partners which cansynthesizesecondarycompoundsthatdeteroraretoxictonaturalen­emies.Awell­knownexampleamongplantsistheprotectionfromher­bivoresgainedbymanygrassesfromalkaloid­producingendophyticfungiintheirtissues(Schardl1996;seealsochapter�,section�.�.3).Theincidence of these symbioses between animals and microorganismsis uncertain, and only a few examples have been explored in detail.TheyincludetheproductionofcompoundsknownasbryostatinsbythebacteriumEndobugulasertula in themarinebryozoanBugulaneri­tina(Davidsonetal.�001)andthepolyketidepederinbyunculturedpseudomonads inbothbeetlesof thegenusPederusandsponges, in­cludingTheonellaswinhoei(Piel�00�;Pieletal.�00�).Thereisevidence,direct forPederusandcircumstantial for thebryozoansandsponges,thatthesecompoundsprotecttheanimalsfrompredators(KellnerandDettner1996;McGovernandHellberg�003).

Thecomplexityof somesymbioses involvingmicroorganismswitha defensive function is illustrated by two highly specific associationsbetweeninsectsandstreptomycetebacteria.Oneistherelationshipbe­tweenbeewolves(beesofthefamilyCrabanidae)andCandidatusStrep­tomycesphilantiilocatedinglandsontheantennaeoftheadultbeewolf(Kaltenpothetal.�005).Theadultfemaletransfersaninoculumofbac­teriatothebroodcell,inwhicheggsaredeposited.Induecourse,thelarvaloffspringcollectthebacteriafromthebroodcellandapplythemto the silk of their cocoonwithinwhich they subsequently pupate inthesoil.Behavioralandbioassaydata indicate that thestreptomyceteproducesantibioticswhichprotectthepupafromfungalattack.Strepto­mycetesarealsocrucialforleaf­cuttingants.Theseantsmaintainfungalgardensofaspecificbasidiomycetefungusonwhichtheantsfeed.ThefungusissusceptibletoaspecificfungalpathogenEscovopsis,andEsco­vopsisinfectionsarekeptincheckbyantibioticsproducedbystreptomy­ceteassociatedwiththeventralsurfaceoftheants(Currieetal.�003).

Bioactive compounds synthesized by a symbiotic partner can alsobeexploited inoffense,as is illustratedbyantlions,predatory larvaeoftheinsectfamilyMyrmeleontidaewithintheorderNeuroptera(thelacewings).Antlionssubduetheirpreybyinjectingtoxicsalivaviatheirpiercing mouthparts. The salivary toxin which paralyzes the prey ofMyrmeleonbore larvae isaprotein,GroEL,producedby thebacterial

18 • Chapter1

symbiontEnterobacteraerogenes(Yoshidaetal.�001).GroELisawell­knownbacterialproteinthatfunctionsasachaperonin,i.e.itpromotesthecorrectfoldingofproteins.ItappearsthattheGroELofE.aerogeneshasadoptedasecondfunctionasatoxinwhileretainingitschaperoninfunction.Fouraminoacidresidueshavebeenidentifiedascritical tothetoxicityoftheprotein;theyareabsentfromtheGroELofotherbac­teria,includingE.coli(theE.coliGroELisnottoxic).ThemodeofactionoftheGroELfromtheantlionsymbiontisnotknown,butitappearstoberelativelyspecificcausingparalysisofotherinsects,includingcock­roaches,butnotofmice.Howtheantlionavoidsthetoxiceffectsoftheproteinisalsounknown.

Somemicrorganismsprotectplantsandanimalsfromtoxicorganiccompoundsandmetalsintheenvironment.Oneofthemostremark­ableexamplesrelatestothepotentneurotoxinmethylmercury,thepol­lutantwhichcausedlarge­scalepoisoningofthehumanpopulationofMinamata, Japan in the 1950s. Methylmercury is absorbed very effi­cientlyacrossthegutwallofanimalsbecauseitformsacomplexwiththeaminoacidcysteinethatmimicsanotheraminoacid,methionine,resulting in its transport throughout the body (Clarkson et al. �003).Bacteria in the gut of mammals can degrade methylmercury by de­methylatingittoelementalmercuryandmercuricions,bothofwhichareeliminatedviathefeces(Rowland1999).Thisreactioninthesym­bioticbacteriahasprovidedpeoplewithadegreeofprotectionagainstmethylmercurycontaminationoffoods.

1.4.3 SymbiosisandtheBiologyofEukaryotes

Theeukaryoticconditionisfundamentallysymbiotic.Thebasisofthisstatementisthatalleukaryoteseitherbearmitochondriaorarederivedfrommitochondriateancestors;andmitochondriahaveevolvedfromsymbioticbacteria.Theevidenceforasymbioticoriginofmitochondriaisoverwhelming.Mitochondriaareproducedexclusivelybydivisionofpreexistingmitochondria,i.e.,eukaryoticcellscannotgeneratemito­chondria de novo, and virtually all mitochondria have their own ge­nomeincludinggenesofsequencealliedtothoseofa­proteobacteria,specifically rickettsias (Gray et al. 1999). Certain anaerobic protistsincluding the diplomonads, metamonads, and microsporidians haveproventobecrucialtoourunderstandingofthecentralityofsymbio­sistoeukaryotes.Theseprotistsbearnostructuresreadilyidentifiablewith mitochondria but, where studied, they have genes of sequencealliedunambiguouslytomitochondrion­derivedgenes.Theinterpreta­tionthattheseorganismshavemitochondriateancestorsissupportedbycarefulcytologicalanalysisrevealingtinymembrane­boundorgan­

TheSignificanceofSymbiosis • 19

elles,knownasmitosomes,withthecharacteristicsofrelictmitochon­dria(e.g.,Tovaretal.�003).

The eukaryote­mitochondrial relationship probably had a singleevolutionaryoriginatleast1.�5billionandperhaps�billionyearsago(EmbleyandMartin�006),meaningthatallmoderneukaryoteshaveevolvedinthecontextofalong­standingintimatesymbiosiswithafor­eignorganism in their cytoplasm.The implicationsare considerable,ascanbeillustratedbyprogrammedcelldeathineukaryotes.Anes­sentialearlystep in thecommitmentofeukaryoticcells todie issig­nalexchangebetweenthecytoplasmandthemitochondrion,resultinginthereleaseofthemitochondrialproteincytochromecfromthemito­chondrialmatrixtothecytoplasm.Whyshouldanorganellewithpri­mary function in aerobic metabolism be central to cell suicide? Onepossibility is that programmed cell death is an evolutionary modifi­cationofantagonisticinteractionsbetweentheeukaryoticnucleocyto­plasmandthebacterialancestorofmitochondria. It isnotsuggestedthatprogrammedcelldeath isanexpressionofvirulence inmodernmitochondria,butthatthecentralroleofmitochondriainprogrammedcelldeathmayhaveevolvedfromsuchaninteraction.Iconsiderthisinteraction further in thecontextof theevolutionofmitochondria inchapter3,section3.6.3.

Itiswidelyacceptedthattheselectiveadvantagetotheeukaryoteofassociatingwith thebacterialancestorofmitochondriawasaccess tothebacterialtraitofaerobicrespiration.TheancestraleukaryotesalsoapparentlycouldnotfixinorganiccarbonfromCO� ornitrogenfromelementalnitrogen,N�.Variouseukaryoticlineageshaverepeatedlyac­quired these lattercapabilitiesbysymbiosiswithbacteriapossessingthesecapabilities.Theplastids/chloroplastsofallphotosyntheticeu­karyotes(theplantsandalgae)arederivedultimatelyfromsymbioticcyanobacteria capable of oxygenic photosynthesis. There are varioussymbiosesbetweeneukaryotesandnitrogen­fixingbacteria(Kneipetal.�007),butwehavenoentirelysatisfactoryexplanationfortheap­parentabsenceofnitrogen­fixingorganellesineukaryotes(seechapter3,section3.6.5).

1.4.4 SymbiosisandtheEcologicalSignificanceofSomePlantsandAnimals

Plantsandanimalsliveinamicrobialworld.Theirsurfacesarecolonizedbymicroorganisms(bacteriaandprotists) fromwhichtheygenerallyderivenosubstantialharm.Someplantsandanimals,however,liveinspecificandcoevolvedrelationshipswithparticularmicroorganisms,and these associations have profound impacts on the ecology and

�0 • Chapter1

evolutionof the taxa involvedand, in some instances,alsoonentireecosystems.Inparticular,animalorplantsymbioseswithmicroorgan­ismsdominatemostterrestriallandscapes,certaincoastalenvironmentsandtheimmediateenvironsofdeep­seahydrothermalvents.

The roots of more than 75% of plant taxa are susceptible to infec­tionbymycorrhizal fungi(NewmanandReddell1987)whichgener­ally promote plant mineral nutrition. Molecular and paleontologicaldatasuggestthattheassociationwithonetypeofmycorrhizalfungi,the arbuscular mycorrhizal fungi, is very ancient, probably evolvingca.�00millionyearsagoatthetimeoftheoriginoflandplants(Simonetal.1993).Ithasbeenarguedthatthesymbiosisandtheresultanten­hancedcapacityofearlyplantstoacquirenutrientsfromthesubstra­tumwasaprerequisitefortheevolutionarytransitionofplantsfromaquatictoterrestrialhabitats.Furthermore,thesefungiproduceagly­coproteinknownasglomalinwhichcanaccountforupto5%ofsoilcarbonandnitrogenandpromotessoilstructure(Rillig�00�;TresederandTurner�007).Theimplicationis that, ifmycorrhizalassociationshadnotevolved,thenterrestriallandscapeswouldprobablyhavebeendominatedbymicrobialmatsandcrusts,especiallyofcyanobacteria.Certainly,mycorrhizalinfectionisthenorminthevegetationinmosthabitatstoday,includingtropicalrainforests,temperateandborealfor­ests, savannah,and temperategrasslands (TresederandCross�006).Oneimportanttypeofvegetationthatisnotfoundedonmycorrhizasislandusedforannualcropproduction,whereplowingandrelatedprac­ticesgenerateahighlydisturbedsoilenvironmentinwhichmycorrhizalfungalnetworkscannotestablishfully.Thisisonefactorcontributingtotherequirementofconventionalcropproductionforhighnutrientinputs.

Wave­resistantcalcareousreefsareacharacteristicfeatureofmanyshallow,clearwatersatlowlatitudes(<ca.35˚).Althoughthesereefsaccountforjust�%oftheareaofcoastalwaters,theyareofimmenseecologicalandeconomicimportance.Theyarerenownedasecosystemsof high biodiversity and productivity, and they support fishing andtourismindustriescrucialtotheeconomyofmanycountries,aswellasprovidingcoastaldefenseagainststorms(Cesaretal.�003).Thereefsaregeneratedpredominantly from the skeletonsof scleractiniancor­alsbearingdinoflagellatemicroalgaeofthegenusSymbiodinium(alsoknown as zooxanthellae) in their tissues; and there is strong experi­mental evidence that coral skeletogenesis by shallow­water corals ispromoted by the photosynthetic activity of the zooxanthellae (Moyaetal.�006).Thecoral­zooxanthellasymbiosisis,thus,thearchitecturalfoundationofshallow­watercoralreefecosystems.Furthermore,thereisevidencethatreefbuildingbyscleractiniancoralsinshallowwaters

TheSignificanceofSymbiosis • �1

dependedonthepriorevolutionof thealgalsymbiosis.This issue isconsideredfurtherinchapter5(section5.�.1).

The importanceofmicrobialsymbioses inshapingecologicalcom­munitiesisalsoillustratedbythefaunaassociatedwithdeep­seahy­drothermalvents,wherehotwatersenrichedwithreducedinorganiccompounds are released into the water column at areas of sea floorspreading.Onewouldexpectsuchhabitatstobedominatedbymicro­organisms, especially chemoautotrophic bacteria which can harnessthe energy generated by oxidation of reduced inorganic compoundstocarbondioxidefixation.Mosthydrothermalvents,however,arealsorichlycolonizedbyadiverseinvertebratefauna,insomelocationsin­cludingvestimentiferantube­wormsupto�mlongandlargebivalvemollusks.Thebasisofthisexceptionalfaunaissymbiosis:theanimalsderive fixed carbon compounds from chemoautotrophic bacteria intheirtissues(VanDover�000).Thesecommunitiesareuniqueintheirindependencefromsolarenergy.Theycouldpersistformilleniaintheabsenceofthesun(butnotindefinitelybecausetheyrequireoxygen,derivedultimately fromoxygenicphotosynthesis).Taxonomicallyal­liedwormsandbivalvesalsooccurinmarinesediments,hydrocarbonseeps,andwhalefalls,i.e.,thedecayingcarcassesofwhalesontheseabottom(VanDover�000;BacoandSmith�003).Symbiosiswithchemo­autotrophshasexpandedthemetabolicrepertoireoftheseanimals,en­ablingthemtoexploithabitatsthatwouldotherwisebeavailableonlytomicroorganisms.

Inadditiontothemanysymbioseswithmicroorganisms,awidedi­versityofanimalsandplantsassociatewithotheranimals,e.g.,mitesandantswithplants;shrimps,crabs,andfishwithcoralsandseaanem­ones.Thesesymbioseshavetraditionallybeentreatedasecologicallytrivialbutusefulmodelsystemstostudythebehavioralandmorpho­logical consequences of coevolutionary processes and biological spe­cialization.Recentresearchonbothsomemarinerelationshipsandantassociationswithplantsandhemipteraninsectssuggeststhattheseas­sociations are of far greater ecological significance than traditionallybelieved. In particular, some have substantial impacts on the widercommunitystructure,includingthepromotionofspeciesdiversity(e.g.,HeilandMcKey�003;Hayetal.�00�).

1.5 The Structure of This Book

In this chapter, I have introduced and illustrated two key points.First,weliveinasymbiosis­richworld,inwhichthesymbiotichabitiswidespreadandabundant.Second,symbiosescontributetothereal

�� • Chapter1

complexityandvariabilityinbioticinteractions.Inparticular,theprev­alenceofsymbiosesdemonstratesthatthenaturalworldisnotdrivenexclusively by antagonistic interactions; and the acquisition of noveltraitsbysymbiosisisanimportantexceptiontothegeneralitythatevo­lutionarychangeismediatedbymultiple,sequentialmutations,eachwithasmallphenotypiceffect.Altogether,symbiosisisabiologicalphe­nomenonoffirst­orderimportance.

As stated at the beginning of this chapter, the central purpose ofthisbookis toexplorethesymbiotichabit, includinghowsymbiosesare formed and persist in both evolutionary and physiological time.Symbiosesposegenuinebiologicalproblems.Asthemanytwentieth­century biologists who regarded symbioses as trivial would argue,symbiosisappears tobe improbablebecause thebenefits thatsymbi­oticorganismsconferontheirpartnersareoftencostlytoprovide,andtheparticipantsoftencompeteforacommonresource.Howisitthat,despitetheseconflicts,symbiosesareprevalentandpersistent?Thean­swercomesinthreeparts,exploredinchapters�–�.

Inchapter�,“TheEvolutionaryOriginsandFatesofOrganismsinSymbiosis,” I consider the evolutionary relationships between sym­biotic organisms and organisms with different lifestyles. It is widelyassumed, especially among biologists modeling the evolution of co­operationandsymbiosis(e.g., JohnstoneandBshary,�00�;Hauertetal.,�006;TraulsenandNovak�006;Tayloretal.�007)thatsymbioseshaveevolvedfromantagonisticrelationshipsandarepronetoreverttoantagonism.Thereviewoftheevolutionaryhistoryofsymbiosesinchapter�yieldsaverydifferentpicture.Althoughevolutionarytransi­tionsbetweenantagonisticandmutualisticrelationshipscertainlyhaveoccurred,theevolutionaryoriginsofsymbiosesarediverse,andmanyrealsymbiosesarederivedfromcasualrelationshipsorinvolvemutu­alistsderivedfromdifferentsymbioses.

Whatever the evolutionary origin of symbioses, their persistenceimplies that conflicts among the partners do not necessarily lead tosymbiosisbreakdownwithinthelifespanofanindividualorganismorovershortevolutionarytimescales.Inchapter3,“ConflictandConflictResolution,”Ireviewtheincidenceofconflictandsomeoftheroutesbywhichconflictcanbemanaged.Potentiallywidespreadmechanismsofconflictresolutioninvolveasymmetryamongthesymbioticorganisms,with one in control and enforcing the good behavior of its partners.Althoughsymbiosesaremutualistic,theyarenotnecessarilycoopera­tives of coequals. This is illustrated particularly by organelles thatare controlled almost totally by the host. I argue that the evolution­arytransitiontoorganellesistheconsequenceofoneroutetoconflictresolution.

TheSignificanceofSymbiosis • �3

Conflict among organisms in symbiosis is heightened when onepartnerfailstoprovideaserviceorconsumescommonresourcesex­cessively. Symbiotic organisms that avoid such unsuitable partnersareexpectedtoencounterlowerlevelsofconflictwiththeirpartners.Partnerchoiceisasufficientlyimportanttopictomeritafullchapteron itsown. Inchapter�,“ChoosingandChosen inSymbiosis,” Iex­plorethemechanismsbywhichorganismsidentifycooperativepart­ners,discriminateagainstineffectiveorganismsandpersisttogetherinapparentharmony.Manyoftheputativemechanismsarewidelyper­ceived as preexisting defenses against antagonists that are recruited,often with modification, for symbiotic function. However, with therecognitionoftheantiquityandpervasivenessofthesymbiotichabit,weshouldconsideralternativepossibilities.Perhaps,mechanismsthathave evolved for the management of organismal interactions can beappliedtobothbeneficialandantagonisticrelationships;andtheyarelabeledasdefensiveresponsesonlybecauseofthegreaterresearchef­fortonantagonisticthanonmutualisticassociations.

Inchapter5,“TheSuccessofSymbiosis,”Iapplyunderstandingoftheformationandpersistenceofsymbioses,asexploredinchapters�–�,toinvestigatethebasisofthesignificanceofthesymbiotichabit.Symbi­osesareimportantnotjustbecausetheyarewidespreadandabundant(asconsideredinthischapter)butalsobecausetheacquisitionofsym­biosiscandramaticallyaltertheevolutionaryhistoryofsomelineagesandchangethestructureofecologicalcommunities.Ialsoconsiderthesuccessofsymbiosesinthecontextofhumanactivities.Thereareboththreatsandopportunities:threatstosymbiosesarisingfromanthropo­genicimpacts,andopportunitieswherewecanharnesssymbiosestoouradvantage,especiallyinmedicineandpestcontrolstrategies.Under­standingoftheprocessesunderlyingthesymbiotichabit(chapters�–�)cancontributetotheameliorationof thesethreatsandthesuccessfulexploitationofvariousassociations.

Intheconcludingchapter6,“Perspectives,”Iexploretheopportu­nityforfutureresearchonsymbiosisandsomeoutstandingquestionsthatcanberesolvedbestbyanalysisacrossmanysymbioses.

Thestructureofthisbookisfoundedontheperspectivethatagraspofmultiplesystemscanpromoteourunderstandingofthesymbiotichabit.MostofthesystemsthatIusetoillustrateanddevelopthemesaresymbioses,but Ialsoaddressparasiticorpathogenic interactionsandnonpersistentmutualisticrelationshipswheretheycancontributetomyargument.