the symbiotic habit - princeton universityassets.press.princeton.edu/chapters/s9239.pdfsymbiosis...
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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
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� • 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
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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.
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� • 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
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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
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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
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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
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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,
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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
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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
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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.
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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
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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).
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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)
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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
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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
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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
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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
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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
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�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
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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
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�� • 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.
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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.