FLEXIBILITY AND SPECIFICITY IN CORAL-ALGAL SYMBIOSIS

34 Pages·2005·0.44 MB·English

by  Andrew C. Baker

13Nov2003 23:7 AR AR200-ES34-24.tex AR200-ES34-24.sgm LaTeX2e(2002/01/18) P1:GJB
10.1146/annurev.ecolsys.34.011802.132417
Annu.Rev.Ecol.Evol.Syst.2003.34:661–89
doi:10.1146/annurev.ecolsys.34.011802.132417
Copyright(cid:176)c 2003byAnnualReviews.Allrightsreserved
FirstpublishedonlineasaReviewinAdvanceonAugust6,2003
F S C -A
LEXIBILITY AND PECIFICITY IN ORAL LGAL
SYMBIOSIS: Diversity, Ecology, and Biogeography
of Symbiodinium
g
s.or Andrew C. Baker1,2
w
vie 1WildlifeConservationSociety,MarineConservationProgram,2300SouthernBoulevard,
nualrenly. 2BCroenntxe,rNfeowrEYnovrikro1n0m46e0ntalResearchandConservation,ColumbiaUniversity,MC5557,
no
urnals.anal use 1200AmsterdamAvenue,NewYork,NewYork10027;email:[email protected]
oo
arjers KeyWords bleaching,climatechange,reef,scleractinia,zooxanthellae
om or p
aded fr1/05. F “Wwhhaatteevveerriissflriegxiidbalendanbdloflcokwedinwgilwliwllittheenrdatnodgdrioew,”,
o3
nl2/ —TaoTeChing
w1
1-689. Doversity on TanhgerAoseubpssytormfaebcxitocnetpRsteiaoernfeacclolryritaidlcsiavl(eacrnsoedmdopitnohoneflernamtgseaolrlifantceeoisrnyavlmerrbetieeofbnretacstoeinssyatshnteedmgpesrnowutishsotSssy)emalbroeisoshdodinsutirsuinmtog.
34:66n Uni stress-related“bleaching”eventscanleadtomassmortalityofcoralhostsandassoci-
03.gto atedcollapseofreefecosystems.Molecularstudieshaveshownthesepartnershipsto
0n bemoreflexiblethanpreviouslythought,withdifferenthostsandsymbiontsshowing
yst. 2Washi varying degrees of specificity in their associations. Further studies are beginning to
col. Evol. Sy Western riutthenyve.ceolUaomlnnmutghs-oetuenarslmyhssoytrsemetmsbtiaaliixoteiancn,t,csoeenrcoooafrltmoclgoaairtlcialtaylulr,dfeoiaenunfandledcebooxinostrylgeysemtoienegmsrlasamprtvhoaaiycelnpsuvtranoirgdvoeeensrm,pcimrenitnnaitcriagnaliglnpsianelortfueunntrvhdbiiearsrtosiflnotamnenx.ediTnbinhtislge-,
Eb
v. persistenceofbleaching-resistantsymbionttypesinaffectedecosystems,andthepos-
e
R sibility of recombination among different partners following bleaching, may lead to
u.
n significantshiftsinsymbiontcommunitystructureandelevationsoffuturebleaching
n
A thresholds.Monitoringsymbiontcommunitiesworldwideisessentialtounderstand-
ing the long-term response of reefs to global climate change because it will help
resolve current controversy over the timescales over which symbiont change might
occur. Symbiont diversity should be explicitly incorporated into the design of coral
reefMarineProtectedAreas(MPAs)whereresistanceorresiliencetobleachingisa
consideration.
1543-592X/03/1215-0661$14.00 661
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662 BAKER
INTRODUCTION
Theunicellularalgalsymbiontsfoundinreefcoralsandassociatedreefbiotaare
criticaltounderstandingthepastevolution,presentdistribution,andfuturefateof
coralreefsandtheecosystemstheysupport(Cowen1988,Hoegh-Guldberg1999,
Muscatine & Porter 1977). In fact, despite their fantastic abundance (a healthy
coralreefmighteasilycontain>1010algalsymbiontsperm2),theirrelativelysmall
overallbiomasssuggeststhesesymbiontsrepresentkeystonespecies(Paine1969,
Poweretal.1996)oncoralreefs—perhapstheonlyprotiststoplaysucharole.
g
or Currently, eight genera in four (or five) classical orders of dinoflagellate are
s.
w recognizedasendosymbiontsinmarineinvertebratesandprotists(Banaszaketal.
e
vi 1993,Trench1997).Symbiodiniumisthemoststudiedgenusinthisparaphyletic
e
nualrnly. groupandiscommonlyfoundinshallowwatertropicalandsubtropicalcnidarians.
no Thesealgae,commonlyreferredtoas“zooxanthellae,”areubiquitousmembersof
urnals.anal use creopraolrtreedefteococsoynsttaeimnsS(yRmobwioadnin1i9u9m8,iTnacylulodre1m97a4n,yTrreenpcrehs1en9t9a3ti)v:eCsnfidroamrianthsepecclaiesss
oo
arjers Anthozoa (including anemones, scleractinian corals, zoanthids, corallimorphs,
om or p blue corals, alcyonacean corals, and sea fans) and several representatives from
aded fr1/05. F t(hineccluladsisnegsmScilylpephoorzionae(fiinreclcuodrianlsg).rhSiyzmobstioomdieniaunmdhcoasroanlsaotebjeeelnlyifidsehn)tiafineddHfryodmrogzaosa-
o3
wnl12/ tropodandbivalvemollusks[includingtridacnid(giant)clams,heartcockles,and
on
Do possibly,conch],largemiliolidforaminifera(inthesubfamilySoritinae),sponges,
1-689. versity aLnodbbaangieatntalh.e2t0er0o2t;riHchillci&liaWteil(csoeexT19re9n8c;han1d99r3efeforernrceevsieiwn;FCigaurrleos1)e.tHalo.w1e9v9e9r;,
34:66n Uni in many of these groups, symbionts have only been definitively identifid from a
03.gto fewrepresentatives;onlyafewgroups(scleractiniancorals,soritidforaminifera,
yst. 20Washin gtooargnoenxitaennst,tahnadtmtriigdhatcbneidcoclnasmidse)rehdavmeabregeinnaslluyrvreepyreedseunstiantgivmeo(Bleackuelrar19te9c9h;nBiqaukeesr
S
col. Evol. y Western &etaRIlt.oi2ws0ac0nl1e;1ar9R9toh7wa;taGnaod&udliePtitoo1wn9ae9lr9sd;i1vL9e9arsJ1ieatuy,bn;ienSssaSenytm2o0bs0ieo2td;aiPnl.aiu2wm0l0or2weasm)k.aiientsatlo. 2b0e0d1i;scPoovcehroedn
Eb
v. (Baker2003)andthatmostspeciesareunculturedandundescribed(Rowan1998,
e
R Santosetal.2001).Manyrecordsof“zooxanthellae”presentininvertebratesare
nu. based on only cursory observations or anecdotal reports. Moreover, in addition
n
A to the dominant populations of symbiotic dinoflagellates in these hosts, many
unusualornovelvariantsmayalsooccurascrypticandunstabletransientswhose
physiologicalorecologicalimportanceisnotyetclear(Goulet&Coffroth1997,
LaJeunesse2001,Santosetal.2001,Tolleretal.2001a).
Thepurposeofthisreviewistosynthesizeresearchofthepastdozenyearsthat
hasusedmolecularDNAtechniquestoquantify,classify,andstudythedistribution
ofdiversityinSymbiodinium.InhisoriginaldescriptionofSymbiodiniummicroad-
riaticum,Freudenthal(1962)observed“asoundtaxonomyofthezooxanthellae—
one taking into account pure-culture studies and host-symbiont specificities—
is needed for ecological work on coral and other zooxanthellae associations.”
13Nov2003 23:7 AR AR200-ES34-24.tex AR200-ES34-24.sgm LaTeX2e(2002/01/18) P1:GJB
FLEXIBILITYINCORAL-ALGALSYMBIOSIS 663
This statement remains a valid motivation for research on Symbiodinium today.
However, with the rise of molecular methods for identification, certain avenues
of research—notably those dealing with partner specificity, biogeography, and
ecology—haveadvancedrapidlyoverthepastfewyearsinwaysthatFreudenthal
could not have anticipated. This review emphasizes how molecular techniques
havebeenappliedtostudyingfield-collectedmaterialfromdiversehosts,environ-
ments,andlocations—anapproachthathasrevolutionizedourunderstandingof
howcomplexandflexibletheseassociationscanbe.Animplicitmotivationbehind
muchofthisresearchhasbeentounderstandtheroleofsymbiontdiversityand/or
org flexibilityindeterminingpossiblelong-andshort-termresponsesofcoralreefsto
ws. environmentalchangeandglobalwarming.Consequently,thisreviewfocusesprin-
e
vi cipallyonscleractiniancoralsymbiosesastheprincipalbuildersofcontemporary
e
nualrnly. coralreefsandthesubjectsofmostoftheresearchundertakenduringthistime.
no
urnals.anal use DIVERSITY,PHYLOGENY,ANDSYSTEMATICSOF
oo SYMBIODINIUM
arjers
aded from 1/05. For p DiverTshiteyrearecurrentlyelevennamedspeciesintheexceptionallydiversegenusSym-
o3
wnl12/ biodinium(Figure1).Allfourformallydescribedspecies(S.microadriaticum,S.
Doon pilosum,S.kawagutii,andS.goreaui)havebeendistinguishedusingthemorpho-
1-689. versity laongdicaaslismpeilcairesractioonncaelpeth(aFsrebuedeennuthsaeld1t9o6n2a,mTereannchad2d0i0ti0o,nTalresnixchsp&ecBielsan(k“S1.9c8a7li)-,
34:66n Uni fornium,”“S.corculorum,”“S.meandrinae,”“S.pulchrorum,”“S.bermudense,”
03.gto and “S. cariborum”) without formal description, although some of these names
yst. 20Washin m(“Say. mbuescsyantionneyi”m)ohuass(bBeaennasdzisatkinegtuiaslh.e1d9s9o3l,elRyofwroamn 1m9o9l8e)c.uAlarfsuerqthueerncsepedcaietas
S
col. Evol. y Western (lbiLenauaJcehmueneaemesbs(eeTrr&eonfcTthrhee&ncghTenh2ui0ns0hS0y1).m99Ibn5io)adidisdniaitulismoon,(rLetchaoJeegudnneizsecesrdsie,boe2dn00sm1po,elcWeiceiuslclaoGrxygm1r9no9ou8dn)id,nsia,untmod
Eb
v. anadditionalSymbiodiniumspecies(closelyrelatedto“S.californium”)hasbeen
e
R misidentifiedasGymnodiniumvarians(LaJeunesse&Trench2000).
nu. Lack of observed sexual reproduction in this group precludes the use of the
n
A biologicalspeciesconcepttodefinespeciesboundaries,althoughvariousgenetic
measuressuggestthesemicroalgaereproducesexually(Baillieetal.1998,2000b;
Belda-Baillie et al. 1999; Goulet & Coffroth 1997; LaJeunesse 2001; Santos
et al. 2003b; Schoenberg & Trench 1980a). In documenting diversity in Sym-
biodinium,problemsrecognizingdistinctspecieshavebeencompoundedbydif-
ficulties associated with the need to culture these microalgae for morphological
description.However,increasingsuccessinrecognizingdiversityusingmolecu-
lar methods has resulted in the de facto use of the phylogenetic species concept
(Eldredge&Cracraft1980)todistinguishtaxa,particularlywhentheyalsohave
distinctecologicalorhost-specificdistributions.Manyofthemoleculartypesthus
13Nov2003 23:7 AR AR200-ES34-24.tex AR200-ES34-24.sgm LaTeX2e(2002/01/18) P1:GJB
664 BAKER
identifiedareseparatedbygeneticdistancesthataremanytimesthosefoundsepa-
ratingrecognizedspeciesoffree-livingdinoflagellates.Consequently,ajustifiable
argumenthasbeenmadethatthegenusSymbiodiniumisspeciose(Blank&Trench
1985a,b;Rowan1998;Rowan&Powers1992),consistingofseveralmajorclades
orlineages(“subgenera”)eachcontainingmultiplespecies.However,theuseof
sequencedatatodefinespeciesboundariesmaywellbeconfoundedbythehighly
unusualnuclearcharacteristicsofthesedinoflagellates(e.g.,Rizzo1987)andtheir
probablyhaploidnature(Santos&Coffroth2003),makinganyinformativecon-
clusionsprematureatthisstage.
org Insufficientsamplingalsohindersourabilitytodetermineexactlyhowmany
ws. “species”existwithineachoftheprincipalSymbiodiniumclades.Therateofdis-
e
vi coveryofnovelmoleculartypescontinuestoincreaserapidly(Baker2003)with
e
nualrnly. currentestimatesreaching100ormore(LaJeunesse2001,2002;LaJeunesseetal.
no 2003;T.C.LaJeunesse,unpublisheddata)eachofwhichLaJeunesse(2001)con-
urnals.anal use sMid.Aer.sCdiosftifnrocttha,ttshuebmspiettceidesmleavneuls[cbruitpst,eefoSr.Re.vSidaenntocse,Tof.Le.vSehneafirenre,rAs.uRb.dHivainsnioens,,
oo
arjers and Rodriguez-Lanetty (2003) for a quantitative estimate of lineage diversity].
om or p At even finer taxonomic resolution, isozymes, randomly amplified polymorphic
aded fr1/05. F DpoNpAula(tRioAnP-lDevse),lvDaNriAabifilintygeirnpSriynmtibnigo,dainnidummi(cBraoislaliteeleltitaels.1h9av9e8,r2e0p0o0rtbe;dGeoxutrleetm&e
o3
nl2/ Coffroth1997,2003a,b)andhavedemonstratedthathundredsofuniquegenotypes
w1
Doon mayexistforeachofthetaxadistinguishedtodate(Santos&Coffroth2003).
1-689. versity
34:66n Uni Phylogeny
03.gto MolecularphylogeniesofSymbiodiniumhavebeendominatedbytheuseofnu-
yst. 20Washin crilbeoarsogmenaelssmenacllosduibnugnriitb(oSsSoUm)a(lBRroNwAn(entraDl.N2A00).2aT,hCeaserlostsuedtiaels.1h9av9e9,iDncalruiduesdettahle.
S
col. Evol. y Western 212090090092,,aR,LTooowhllaeenrt&2a0lP.0o21w0b0,eV1rs,a1nP9aO9wp2lp,oSewnasdekltiearele.tt2aa0ll.0.1129,0W9021i),l,cPpooaxcr1thi9ao9lnl8ae)r,tgaeanls.du2ibn0ut0en1rint,(aSLlaStvrUaang)se(cBreiatbkaeeldr.
Eb
v. spacers(ITS1and2)and5.8Sregions(Brownetal.2000,2002;Hunteretal.1997;
e
R LaJeunesse2001,2002;LaJeunesseetal.2003;Savageetal.2002a;VanOppen
nu. et al. 2001). Recently, partial LSU chloroplast rDNA (cprDNA) sequences have
n
A been used to independently test the relationships inferred from nrDNA (Santos
etal.2002a,b,2003a).
Together, these studies have recognized between four and ten distinct clades
ofSymbiodinium.Despitedifferencesinthephylogeneticdiversityofsourcema-
terial and semantic disagreement over which clades deserve their own name, a
surprisingdegreeofcongruencebetweenthesephylogeniesexists.Inparticular,
theindependentorganellarmarker(LSUcprDNA)usedbySantosetal.(2002a)
recovered a phylogeny that was not significantly different from established
nrDNAphylogenies,althoughsomeuncertaintyintherelativepositionsofclades
B, C, and F was indicated (Baker 1999, Carlos et al. 1999, Darius et al. 2000,
13Nov2003 23:7 AR AR200-ES34-24.tex AR200-ES34-24.sgm LaTeX2e(2002/01/18) P1:GJB
FLEXIBILITYINCORAL-ALGALSYMBIOSIS 665
LaJeunesse 2001, Loh et al. 2001, Pawlowski et al. 2001, Pochon et al. 2001,
Rowan&Powers1992,Savageetal.2002a,VanOppenetal.2001,Wilcox1998).
Congruentdatasetsfromindependentnuclearandorganellarsourcesstronglysup-
portthephylogenypresentedinFigure1,whichrecognizessevendistinctclades
(AthroughG)andfollowsnomenclatureestablishedbyRowan&Powers(1991b),
Baker (1999), Carlos et al. (1999), LaJeunesse & Trench (2000), Pochon et al.
(2001),andRodriguez-Lanetty(2003).SymbiodiniumF,astheleastwell-resolved
clade,wouldbenefitfromfurtheranalysistodeterminethesupportforitshighly
divergentmembers(seeRodriguez-Lanetty2003),includingS.kawagutii,which
org earlierreportshadplacedincladeC(e.g.,Banaszaketal.2000,Carlosetal.1999,
ws. Santosetal.2001).
e
vi
e
nualrnly. SystematicsandNomenclature
no
urnals.anal use Tplhoeyeudsebfyulinnedsespoenfdaenntaamuethiosrsr.elIinabthlyisrceoflnetcetxetd,tbhyeathrbeiterxatreynAt,toB,wahnidchCiStyims bemio--
oo
arjers diniumclassificationsystemintroducedbyRowan&Powers(1991b)hasproved
om or p remarkablyuseful:AllmolecularstudiesofSymbiodiniumpublishedtodatehave
aded fr1/05. F edmisapgloreyeemdethnet osvamerethneomexepnacnlastiuorneotfoRreofweranto&thPeoswameres’li(n1e9a9g1ebs).Horoigwienvaelrn,oremceenn-t
o3
wnl12/ clature to include Symbiodinium diversity not named by them has led to some
Doon confusion.
1-689. versity to aThgirsoucopnofufssioynmbceionntetsrsfoauronudndinthCeariinbtbroeadnucsticolenraocftiSnyiamnbicoodrianlsiu(mToElletroertefaelr.
34:66n Uni 2001a,b)—a practice followed by Goodson (2000), Brown et al. (2000, 2002a),
03.gto Savage et al. (2002a), and Chen et al. (2003a,b) for corals containing similar
yst. 20Washin sSyymmbbiioodnitnsifurmomDThhaadilbaenedn, Sust.edCrboyixC,aTraloiwsaent,ala.n(d19H9o9n)gtoKroefnegr.tRoeacnougnnuizsiunaglitshoa-t
S
col. Evol. y Western olnafetwepalfyrrtodiamilscLtohSveUeirnestdeeqrsusytemintibcaeiloswnftraottyempreobsfoatashSsnpyumocnlbegiaoer,daiTnnoidullmecrhEleo.trHoaplo.lwa(2setv0er0Dr1,Nas,eAbq)u(dePinosctciehnaognnuaieslythsaeilds.
Eb
v. 2001,Santosetal.2002a)revealthatthesymbiontsreferredtoasSymbiodinium
e
R EbyTolleretal.(2001a,b)aredistantlyrelatedmembersofthesamecladeasthe
nu. D-typeoriginallyidentifiedbyCarlosetal.(1999),afindingsupportedbyaddi-
n
A tionalanalysis(X.Pochon,unpublisheddata).Ironically,thislineageofsymbionts
wasapparentlydocumentedfromaHawaiianscleractiniancoralinRowan&Pow-
ers’ (1991b) original phylogeny, but it was not given a name and no sequence
data were provided. Carlos et al. (1999) determined that the sponge isolate and
the unusual coral symbiont of Rowan & Powers (1991b) shared a similar RFLP
genotype,lendingfurthersupporttotheconclusionthattheybelongtothesame
clade.
While the naming of clades is wholly a question of semantics, and deciding
whichcladesareworthyofnameswithinanemergingphylogenyofSymbiodinium
isasomewhatarbitraryprocess,nameshavevalueonlyifusedconsistently.The
13Nov2003 23:7 AR AR200-ES34-24.tex AR200-ES34-24.sgm LaTeX2e(2002/01/18) P1:GJB
666 BAKER
recommendation made here follows the practice of Baker (1999, 2001, 2003),
Glynnetal.(2001),LaJeunesse(2001,2002),Lohetal.(2001),Pawlowskietal.
(2001), Pochon et al. (2001), Van Oppen et al. (2001), Santos et al. (2002a,b;
2003a), and LaJeunesse et al. (2003), Ulstrup & Van Oppen (2003), Van Oppen
(2003),inusingSymbiodiniumDtorefertothesinglecladethatincludesboththe
unusualspongeisolateidentifiedasDbyCarlosetal.(1999)andthesymbionts
of certain scleractinian corals originally referred to as D by Baker (1999) and
subsequently referred to as E by Toller (2001a,b). Symbiodinium E is used to
refer to the clade that includes temperate symbionts isolated from Californian
org Anthopleuranamed“S.californium,”andafree-livingdinoflagellatemisidentified
ws. asGymnodiniumvariansculturedfromawatersampletakenfromWellington,New
vie Zealand(41–S)(LaJeunesse&Trench2000).
e
nualrnly. HowdiversearetheprincipalcladesofSymbiodinium,andhowaretaxawithin
no thesecladesrelatedtooneanother?ThemostcomprehensiveSymbiodiniumphy-
urnals.anal use lsougcecnesiessfutloidnatuesi(nPgawLlSoUwsnkriDetNaAl.2to00id1e,nPtoifcyhovnareiattaiol.n20w0i1th)ihnaavlelbSeyemnbrieoldaitniviuelmy
oo
arjers clades except B and E. However, the phylogenetic structure of this variation is
om or p notwell-resolved.Inparticular,alargeclusterofcloselyrelatedB-andC-types
aded fr1/05. F tdhaattasheatvse(Balaskoerbe1e9n99d,ifDfiacruilutstoetdails.ti2n0g0u0is,hRionwoatnhe&rnPuocwleearsr1S9S9U1ba,nWdLilcSoUxr1D9N98A)
o3
nl2/ remainsunresolvedintheseanalyses.Theextremenumberofsequencevariants
w1
Doon in Symbiodinium C led Baker (1999) and Toller et al. (2001a) to conclude that
1-689. versity aseltnhtoeudgahrtdifiaffcetsreonftcClo-ntyinpges(Sdipdekexsnisitjdweirtehtinalt.h2i0s0c1la)daen,dm/ourcphaorafltohgeovuasrgiaetnioesnwreipthrein-
34:66n Uni therDNArepeat(Rowan&Powers1991a,b).
03.gto Morerecently,sequenceanalysisofmorerapidlyevolvingnuclearITSnrDNA
yst. 20Washin speaqlucelandceess (h“assubregseonlevread”)aodfdiStyiomnbailopdhinyiluomge(nLeatiJceusntreuscsteur2e00w1i,th2i0n0a2l;lLthaJeeupnrienscsie-
S
col. Evol. y Western eAvtalratihla.on2ut0sg0,hL3o;anRJeeoudsnureibgscsuleea(zd2-eL0o0af1n)eCthtyasst2ial0lr0gc3uo;enSdtaativhnaissgaveaenrtiuaamtli.ob2ne0r,0roa2ftah;celVroasthnealOynpbrpeeleianntgeedatrastlei.fqa2uc0et0un1ac)le.,
v. Eb representsrapiddiversificationfromasingleancestraltaxon(Rodriguez-Lanetty
Re 2003;T.C.LaJeunesse,submittedmanuscript).Itnowappearsclearthatsignifi-
nu. cantvariation,noteasilydistinguishedbycloning-basedapproaches,doesindeed
n
A characterizethisandotherclades.
Figure 1 presents a comprehensive analysis of all 294 sequences of the D1-
D2 region of Symbiodinium LSU nrDNA (»650 nt) available in Genbank as of
May 2003. Certain clades not well-resolved in Figure 1 (particularly B, C, and
D, for which many sequences are available) comprise many distinct taxa whose
phylogenetic relationships are not unequivocally resolved in this analysis. Finer
resolutionofdistincttypeswithinthesecladeshasbeenobtainedusingavariety
of molecular screening techniques that include restriction fragment length
polymorphism (RFLP) analysis of SSU and LSU nrDNA (Baker 1999;
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FLEXIBILITYINCORAL-ALGALSYMBIOSIS 667
Bakeretal.1997;Chenetal.2003a,b;Glynnetal.2001;Lohetal.1998,2001;
Pochonetal.2001;Rowan&Powers1991a,b,1992;Tolleretal.2001a,b;Wilcox
1998), temperature gradient gel electrophoresis (TGGE), and denaturing gradi-
entgelelectrophoresis(DGGE)ofSSUnrDNA(Belda-Baillieetal.2002,Carlos
et al. 2000), DGGE analysis of ITS and 5.8S nrDNA (Baillie et al. 2000a;
LaJeunesse 2001, 2002; LaJeunesse et al. 2003), single strand conformational
polymorphism(SSCP)analysisofITSnrDNA(Ulstrup&VanOppen2003,Van
Oppen2003,VanOppenetal.2001),lengthheteroplasmyofLSUcprDNA(Santos
et al. 2001, 2002a,b, 2003a) and phylogenetic analysis of microsatellite flank-
org ing regions (S.R. Santos, T.L. Shearer, A.R. Hannes, M.A. Coffroth, submitted
ws. manuscript). An unfortunate consequence of the variety of different molecular
e
vi markers and methods used in these Symbiodinium surveys is that direct com-
e
nualrnly. parisons of different datasets are not possible. A collaborative multiple-marker
no study of the diverse symbiont types thus far identified would be the only way
urnals.anal use tnoompreoncceleadturien.establishing a truly comprehensive phylogeny and a consensual
oo
arjers HowdogeneticallydifferentSymbiodiniumvaryfunctionallyfromoneanother?
om or p Itisclearthatcloselyrelatedsymbionttaxacandiffersignificantlyintheirphysio-
aded fr1/05. F leotgaicl.al1c9a9p6a,c1it9ie9s9()e.agn.d,Chhoasntgseptecaila.l1i9za8t3io;nIgl(eDsiieaks-mParinentoe&t aTlr.e2n0c0h21,9L9a7J;eWunaernsseer
o3
nl2/ 2002),makinggeneralizationsregardingthepropertiesofparticularclades(par-
w1
Doon ticularly the diverse clades A, B, C, and F) is premature at this stage (Good-
1-689. versity sRoonweatna1l9.9280)0.1H,oSwaevvaegre,aestmalo.le2c0u0l2abr;adbvuatnsceeesaimlsporoKvneoowulrtoanbi&lityRtoohdwisetrin2g0u0is3h,
34:66n Uni more closely related types, physiological patterns not apparent in earlier molec-
03.gto ular studies (e.g., Savage et al. 2002b) may become apparent (e.g., Santos et al.
yst. 20Washin 2tu0r0e2rae)s.eFaurcnhctwiohnoasledfiivnedrisnitgysorefmSyaminbbioedyionniudmthreesmcaoipnesoafnaimcopmorptarenhteanvseinvueereovfifeuw-
S
col. Evol. y Western SPECnIoFwI.CITYOFHOSTSANDSYMBIONTS
Eb
v.
e
R
u. SystematicPatternsofSymbiontDistribution
n
n
A AnoverviewofthedistributionoftheprincipalcladesandsubcladesofSymbio-
diniumreportedfromdifferenthosttaxaisshowninFigure1.Fromthisdistribu-
tional dataset it is clear that associations between Symbiodinium and its various
invertebrate and protist hosts exhibit specificity (sensu Dubos & Kessler 1963):
patternsofassociationareclearlynonrandomandtheratioofobservedcombina-
tions of hosts and symbionts compared with the range of possible combinations
is very small (Rowan 1991; Trench 1988, 1992). However, an emerging picture
of considerable flexibility on the part of both hosts and symbionts reveals that
the idea of uniformly strict specificity—in which all hosts exclusively contain
13Nov2003 23:7 AR AR200-ES34-24.tex AR200-ES34-24.sgm LaTeX2e(2002/01/18) P1:GJB
668 BAKER
onlyonesymbionttype—isincorrect(Trench1988,1992,1993,1996).Onerea-
son why the notion of strict specificity may have prevailed for so long is that
Symbiodiniumtaxonomyfromthe1950stotheearly1990sreliedonthemorpho-
logicalstudyofculturedmaterial.CulturingSymbiodiniumreducesthediversityof
heterogeneousisolates,favoringnonrepresentativemembersoverpreviouslydom-
inant types (Santos et al. 2001). Early conclusions of strict symbiont specificity
maythereforehavebeenpartlytheresultofalong-termculturethatreducedthe
diversity of the original isolate to a single algal genotype that was mistakenly
identifiedas“the”symbiontofaparticularhostspecies.
org Scleractiniancoralsareamongthemostflexiblehostsidentifiedtodate,con-
ws. taining symbionts from clades A, B, C, D, and F. However, this relative high
e
vi diversitymaybeanartifactofsamplingforthesewell-studiedhosts.Benthicsori-
e
nualrnly. tid foraminifera also show remarkable diversity, containing symbionts in clades
no C, F, and G. Anemones of various kinds show considerable symbiont diversity
urnals.anal use D(m),emmiblleerpsoorfincelafidreescAo,raBls,C(m,eDm,banerdsEof),Aa,sBd,oanzdoaCn)t,hainddst(rmideamcnbiedrscloafmAs,(Bm,eCm,baenrds
oo
arjers ofAandC).(SeeFigure1.)
om or p Therelativeeasewithwhichdiversesymbiontshavebeenfoundinmanydif-
aded fr1/05. F f(epreernhtaphsosatlsl)suhgogsetsttasxtahaatrewaebcleantnootasassocyieatterewjeictththmeonreultlhhaynpoontheestyispethaotfmSyamny-
o3
nl2/ biodinium. Laboratory infection experiments suggest that hosts can become in-
w1
Doon fectedwithawidevarietyofdifferentsymbionts(Fitt1984,1985b;Schoenberg&
1-689. versity Tofre(nocfthen19u8n0ucs)u,aaln)dmtihneorfascytmthbaiotnhtosswtsitihninnaatugreencearanllaylshoocmoongtaeinneosmusalplonpuumlabtieorns
34:66n Uni of “normal” symbiont types suggests that what we perceive as specificity may
03.gto be perhaps no more than the end result of competitive exclusion between sym-
yst. 20Washin bmioayntbse(Gproeudloemt &inaCnotlfyfrfortehe-1li9v9in7g, LSayJmebuinoedsisneiu2m00t2h)a.tSaoremmeeorfeltyhe“smeomoninliogrhttyinpge”s
S
col. Evol. y Western acSsaannsytoomcscbeaitosainlo.tns2—a0ll0tyh1e)e.ymWneeervgseehroadusoldmthbieneadctooemnisniendraivvnaittdisuvpeaelicnhioeinssttseinrupncrdeutelitrnugnreaotb(uLsraealrJveceuodnnedpsiatstietoenr2ns0sb0ou2ft,
v. Eb associationasrepresentingthefullrangeofpossiblecombinations.Byimplicitly
Re recognizing specificity as a continuous variable we can distinguish which sym-
nu. biontsareprobable(oftendominantinahost)fromwhichsymbiontsareonlypos-
n
A sible(rareinahost,butpossiblydominantindifferentcircumstancesordifferent
hosts).Newmolecularmethodsappliedtofield-collectedmaterialarepavingthe
wayforinvestigationsofthiskind(LaJeunesse2001,2002;LaJeunesseetal.2003;
Santosetal.2003a;S.R.Santos,T.L.Shearer,A.R.Hannes,M.A.Coffroth,sub-
mittedmanuscript).Additionally,unusualtypesarisinginculturecanfortuitously
assistusinourtaskofrecoveringacomprehensivephylogenyofSymbiodinium.
Forexample,Santosetal.(2003c)culturedanuncommonSymbiodiniumDfrom
ananemoneisolatethatmaynotberepresentativeofitsdominantpopulationsin
hospite.
13Nov2003 23:7 AR AR200-ES34-24.tex AR200-ES34-24.sgm LaTeX2e(2002/01/18) P1:GJB
FLEXIBILITYINCORAL-ALGALSYMBIOSIS 669
HostSpecificityVersusSymbiontSpecificity
A new understanding arising largely from the application of molecular genetics
suggests that some coral hosts are able to associate with a variety of distantly
relatedsymbionttypes,whileothersareapparentlyrestrictedtoasinglesymbiont
typeorsubsetofcloselyrelatedtypes.Similarly,somealgalsymbiontsarewidely
distributedandfoundinmanyhosts(“generalists”),whileothersappearendemic
toparticularlocationsandmayberestrictedtoaparticularhosttaxon(“special-
ists”)(Rowan1998,Baker1999,Tolleretal.2001b,LaJeunesse2002).Weshould
g thereforedistinguishbetweenhostspecificity(thespecificityofhostsforapartic-
or
s. ularrangeofsymbionts)andsymbiontspecificity(thespecificityofsymbiontsfor
w
vie aparticularrangeofhosts).Ingeneral,hostsappearmorespecificthansymbionts:
nualrenly. tthheanmtehaenmneuamnbneurmobfecroomfbcionmatbioinnastiinonwshiinchwahigcihveanghivoesntissyfmobuinodntteinsdfsoutondbe(Tle.Css.
no
urnals.anal use LaJAeucnoenscsee,pstuuablmfirtatmedemwoarnkusfcorripcto).ral-algal specificity is illustrated in Figure 2,
arjoerso in which examples (from the scleractinian corals) of all four combinations of
om or p
aded fr1/05. F
o3
nl2/
w1
on
Do
1-689. versity
34:66n Uni
03.gto
0n
yst. 2Washi
S
col. Evol. y Western
Eb
v.
e
R
u.
n
n
A
Figure2 Conceptualframeworkforsymbiosisspecificity.Hostandsymbiontspecificityare
representedascontinuousvariablesrangingfromstrictspecificitytorelativeflexibility(low
specificity).ExamplesofeachtypeofsymbiosisaregivenforSymbiodiniuminCaribbean
scleractinian corals. 1Symbiodinium B6 of LaJeunesse (2002). 2Symbiodinium C12 of
LaJeunesse(2002).
13Nov2003 23:7 AR AR200-ES34-24.tex AR200-ES34-24.sgm LaTeX2e(2002/01/18) P1:GJB
670 BAKER
low and high host and symbiont specificity are represented. One finding which
emerges from classifying symbioses in this way is that a single association can
bebothhighlyflexibleandhighlyspecific,dependingonwhichpartnerisbeing
discussed.Forexample,theCaribbeanfaviidcoralColpophyllianatanshasbeen
foundhosting(atleast)oneC-typeandtwoB-types,oneofwhichappearshighly
specificforColpophyllia(Baker1999,Baker&Rowan1997,LaJeunesse2002).
Thisassociationisthuscomposedofageneralisthostwithlowsymbiontspeci-
ficity,togetherwithtwogeneralistsymbiontsandonehost-specificsymbiont.The
wide range of interaction strategies (Goff 1982) found in Symbiodinium to date
org supportsthenotionthatresultantsymbiosisbenefitsfromgreaterevolutionaryand
ws. ecologicalpotentialthroughflexibility.
e
vi
e
nualrnly. IntraspecificSymbiontDiversity
no
ournals.aonal use Etyxpaemreppleressoefngtepnaertriacluisltahrloysitnstpeerecsietisntghasptaerceiaalbclaesteosc.Aonltthaionumghoirneitthiaalnlyodnoecsuymmebniotendt
arjers inPacificPocillopora(Rowan&Powers1991a),thesignificanceofintraspecific
om or p symbiontdiversitywasfirstrecognizedinlaterstudiesofCaribbeanMontastraea
oaded fr31/05. F (ieRsodwoacnum&eKntneodwflotounr 1d9if9fe5r;eRntowsyamnbeitoanlt.1ta9x9a7;(iTnofloleurredtiaslt.in2c0t0c1laa,dbe)s.TohfeSsyemsbtuiod--
wnl12/ dinium)inthreecloselyrelatedhostspecies,andtheyshowedthatthesesymbionts
on
Do weredistributedwithinsinglehostspecies(andevenwithinsinglecoralcolonies)
34:661-689. n University isenpteeaccli.oe1lso9hg9oi7cs;atilGnlyglymmnuenaltenitpinlaegl.fsuy2lm0w0b1aioy;nsLt(atsaJeexeuanEaecrseoslneoog2wy0c0bo1em,lo2mw0o)0.n2E;(BxLaaamkJeeprule1ns9e9sos9fe,s2ce0lte0ar1al.;cB2ti0na0kia3enr;
03.gto Pawlowskietal.2001;Pochonetal.2001;Santosetal.2001;VanOppen2001).
0n
yst. 2Washi Bcoarkaelsr(s1u9r9v9ey)ecdonfsreormvattihveelCyarreipbobretaend,thfaart3e8asotefr1n07Pascpieficcieasn(d36G%r)eaotfBscalrerriaecrtiRnieaenf
S
col. Evol. y Western ib(nGioBsnuRtrvd)eicvyoesnrsotaiftiynCeiasdrnimbobutelctaoinpnlfireeneSefydmintbovietohrdteeinbsicrualemterastcy(tpLineasiJa,enaucnfioenrsdasilens:g2s0tih0ma2it)l.ahrIansfltrebaxesiepbneilcsitiuyfipcwposiytrhtmeind-
Eb
v. single species of host has been found in foraminiferans (Pawlowski et al. 2001,
e
R Pochonetal.2001),anemones(Santosetal.2003c),gorgonians(Coffrothetal.
u.
n 2001;Santosetal.2003b;S.R.Santos,T.L.Shearer;A.R.Hannes;M.A.Coffroth,
n
A
submittedmanuscript;butseealsoGoulet1999,2003a,b)andhydrocorals(Baker
1999,LaJeunesse2002).
Exactly how deterministic is specificity? Do unusual symbionts occasionally
appearinnormallyhighlyspecifichosts,ordohighlyspecificsymbiontsoccasion-
allycolonizeunusualhosts?Strictlyspecificone-on-onepartnershipsaredifficult
todocumentwithcertaintybecauseitisimpossibletosurveyallhostsinallpossible
environments.Apparentstrictspecificitymaymerelyreflectanestablishedstatus
quoinwhichastableequilibriumhasbeenreached.Disturbance,suchasenviron-
mental change, bleaching, or disease might provide a window for opportunistic
partnershipstobecomeestablished(Baker2001,2002;Rowan1998;Tolleretal.