Table Of ContentReference: Biol. Bull 182: 155-158. (February, 1992)
Allorecognition in Colonial Marine Invertebrates:
Does Selection Favor Fusion with Kin
or Fusion with Self?
MICHAEL FELDGARDEN1 AND PHILIP O. YUND2
1Department ofBiology, Yale University, New Haven, Connecticut 06511 and2Department
ofBiologicalSciences, University ofNew Orleans, New Orleans, Louisiana 70148
Previous analyses ofthe selectiveforces operating on al- chimeric colonies as well. Because all genotypes in a chi-
lorecognitionsystemsincolonialmarineinvertebrateshave mera have access to the production ofgametes (4), one
suggestedthatadvantagestofusion with kin haveselected genotype can functionally parasitize other members of
fortheabilityto recognizeandfuse with relatedcolonies. thechimerabycontributingdisproportionatelytogamete
Whilethisexplanation iscompatible with theobservation production(somaticcellparasitism)(4, 8). Allorecognition
ofaggregated settlement offusible larvae in an ascidian systems are thus thought to function to limit fusion to
species, it isnotcompatible with two otherprominentfea- close relatives, so that the benefits of fusion can be ac-
tures ofallorecognition systems theextensiveallorecog- quired while the potential costs are reduced (2). By re-
nitionallelepolymorphismcommonlyobservedinnatural stricting fusion to close relatives, allorecognition systems
populationsandtherecentlyreportedinstabilityofchimeric may constrain somatic parasitism to benefit a relative of
colonies. We suggest that selection forfusion with self, thevictim, hence reducingthe negativeeffectofparasitism
rather thanfusion with kin, offers a moreparsimonious onavictim'sfitnessviaapositiveeffectoninclusivefitness
explanationforthetwofeatureslistedabove. Consequently, (i.e., kin selection) (2).
selffusion may be a major selectiveforce acting on allo- Fusionwith kin isawell-documentedevent, andhence
recognition systems in colonial invertebrates. kin selection is certainly a potential force acting on allo-
recognition systems. However, we will argue that there is
Colonial marine invertebrates typically possess allore- an additional selective force at work, with the genetic in-
cognition systemsthatcontrol fusion andrejection among dividual as the target ofselection, that is more likely to
conspecific colonies, and such systems are either known explaintwo important featuresofallorecognition systems.
orexpected to be genetically based (1). The broad distri- Althoughourargumentisapplicabletomostcolonialtaxa,
bution ofallorecognition in colonial taxaand the parallels we will focus our discussion on botrylloid ascidians and
between invertebrate allorecognition and the vertebrate hydractiniid hydroids, the twogroups forwhich the most
immune system have spawned considerable interest in complete genetic and mechanistic data on allorecognition
theevolutionofallorecognition systems. Previousanalyses are currently available.
ofthe selective forces at work in allorecognition systems At the heart ofthe kin selection argument are the an-
have suggested that allorecognition mediates thecostsand ticipatedcostsand benefitsoffusion. Weagreecompletely
benefits of fusion with conspecifics (1, 2). Fusion with withthisassessment ofcostsandbenefits, butsuggestthat
conspecifics is expected to confer benefits by increasing allorecognition plays adifferent role aswell to permit a
the size ofthe resulting chimeric colony (1-3), which in colony to obtain the benefits offusion (increased colony
turn decreasesthe susceptibility ofacolonytothe impact size)while completely eliminatingthe potential costs(so-
ofecological processes and increases colony reproductive maticcell parasitism). We suggestthat ratherthan simply
output (4-7). However, potential costs are incurred in reducing the potential cost ofsomatic cell parasitism by
limiting fusion to close kin, selection favorscoloniesthat
Received28June 1991;accepted 22 November 1991. avoidthesecostsaltogetherby recognizingand fusingwith
155
156 M. FELDGARDEN AND P. O. YUND
themselves(selffusion). Although fusion between kin oc- In further evaluating the relative impact ofselection for
curs, such events may simply represent mistakes in rec- kin and self fusion, we will discuss the compatibility of
ognition due to the limitations ofan imperfect system. If thesedifferentselectiveforceswiththreedocumented fea-
kin fusion events are artifacts ofallorecognition, kin se- tures of allorecognition systems in botrylloid ascidians
lection need not provide the dominant selective force and hydractiniid hydroids the extreme polymorphism
shaping allorecognition systems. Note that selection for of allorecognition alleles, the instability of chimeras
both selfand kin fusion is generated by the potential for formed by the fusion ofrelated colonies, and the aggre-
somatic cell parasitism. While fusion with kin will limit gated settlement offusible larvae.
this cost, fusion with selfwill prevent it altogether. High levels ofallotypediversityareaprominent feature
Why would autogeneic fusion (fusion with the same ofallorecognition systems in most colonial taxa (1). In
genotype; i.e., self fusion) be selectively favored? Frag- botrylloid ascidians, where the genetic mechanism ofal-
mentation is an ubiquitous feature of colonial inverte- lorecognition is known, allotype diversity isgenerated by
brates, both through controlled fission and as a result of extensive allorecognition allele polymorphism, with the
extrinsic disturbance (9, 1 1). Surviving colony fragments numberofallelesdetected in natural populationsranging
are likely to re-encounter their own genotype upon sub- from 40 to 100 (1, 1 1, 18-20). While the genetics ofal-
sequent growth and lateral expansion. Ifno mechanism lorecognition in hydractiniid hydroids has yet to be fully
for self recognition exists, the subdivided colony will resolved(21,22), fusion eventsandchimericcoloniesap-
compete with itself for space. Hence, autogeneic fusion peartobevery rare in natural populations(23), suggesting
between colony fragmentsconferstheadvantagesboth of a similarly high level ofallele polymorphism.
an increase in size, aspreviously cited, and a release from Several authors have noted that kin selection does not
unnecessary competition. provide an obvious explanation forhigh allotype diversity
While fragmentationandsubsequent re-contactislikely (1, 18, 24, 25). Forhigh levelsofpolymorphism tooccur,
ctoobmemoanmaujnodrersouortcheerofciaructuomgsetnaeniccesfuassionw,ells.elfMfaunsyioncoi-s alleles must increase in frequency when rare. However,
lonial invertebrates (including botrylloid ascidians and kin selection is likely to lead to the elimination of new
alleles, because rare alleles will be involved in few, ifany,
hydractiniid hydroids)growasepibiontson three-dimen-
fusion events (25). Consider the case ofan hypothetical
sional substrata. Consequently, the growing margins ofa
colony frequently encounter selfupon wrapping around new allele arising by mutation. This allele confers no im-
mediate advantage through kin selection, as kin fusion
thesubstratum. Even ifphysiological integration ismain-
tained throughout the intervening regions ofthe colony, eventsattributabletothisalleleare not possible. Selection
themarginal tissue isconfrontedwitharecognition prob- cannot favor the allele until it has already increased in
lem. Asinthecaseoffragmentation,thesecontactsimpose frequency to the point where kin fusion events are likely
a recognize-or-compete constraint on thecolony. In both to occur. Hence, any new allele isat a selective disadvan-
ofthesescenarios, autogeneic fusionconferstheecological tage relative to established allelesand is likely to be elim-
benefitseffusion without thepotential costsofallogeneic inated. Population modelsbasedonthecostsandbenefits
fusion(fusion withothergenotypes;generally kin fusion). ofkin selection (though notexplicitly modeling selection
Early work on the population structure ofcorals and attwolevels)predictthatthe initially most frequentallele
sponges employed allorecognition as an assay ofgenetic will quickly increase to fixation in a population (25).
A
identity and hence explicitly assumed that fusion only closelyrelated problem isthat in orderfortheprem-
occurred amongcoloniesderived from the same genotype isesofkin selection tobe valid, allotype must indicatethe
(i.e., thatall fusion eventswereautogeneic)(12-14). These degreeofrelatednessbetweencolonies. However,thepos-
studies were criticized for failing to provide adequate in- session of a given allorecognition allele is indicative of
dependentverification ofgenotypicidentity(15),andfur- relatedness only when that allele is rare (25). As an allele
ther work suggested that some fusion events were indeed increases in frequency, colonies that share this allele are
allogeneic( 16, 17). Thesubsequent focusontheexistence less likely to have inherited it from a recent common
ofallogeneic fusion may have drawn attention from the ancestor. The sharingofacommon allorecognition allele
potential for autogeneic fusion in nature. While the ex- is thus a very poor assay ofrelatedness. As an allele be-
plicitassumption ofacorrespondence between fusion and comes common, fusion will occur between less related
genetic identity may not have been valid, the implicit as- genotypes, leading to the costsofsomatic cell parasitism.
sumption that allorecognition systems served to permit Due to the failure ofalleles to increase when rare and to
fusion with selfmay well have been accurate. convey accurate information on relatedness, the obser-
To this point, we hope that we have established that vation ofhigh levels ofpolymorphism at allorecognition
the need to recognize and fuse with selftheoretically pro- loci in natural populations is difficult to reconcile with
vides a strong selective force on allorecognition systems. kin selection.
SELECTION FOR SELF FUSION 157
The assumption ofa selective advantage to selffusion might be expected to select against the very existence of
rather than kin fusion alters the selective regime on al- an allorecognition system. Such a system would only be
lorecognition alleles to simple frequency-dependent se- maintained if selectively favored for other reasons; i.e.,
lection. Rare alleles are at a selective advantage due to a the selective advantages to selffusion.
greater potential to correctly identify self, while common LarvaeofB. schlosserisettle in proximitytoboth larvae
allelesareat aselectivedisadvantageduetothepropensity and adult colonies with which they share an allorecog-
to incorrectly identify allogeneic colonies as self. These nition allele and hence can fuse upon subsequent growth
recognition errorsincurforthebearercolonythepotential andcontact(34). Incontrast, H. symbiolongicarpus larvae
costs of fusion (i.e., somatic cell parasitism). Consider settle at random with respect to fusible adults and larvae
again a new allele arising by mutation. This allele is ini- (35). Larval settlement as a function offuture fusibility
tiallyataselectiveadvantage,asitcanberesponsibleonly is the sole observation that we are aware ofthat is con-
for autogeneic fusion events and not for accidental allo- sistentwithkinselectionbutnotwiththeselectivepressure
geneic events. As the allele increases in frequency, the of self fusion. If fusion with relatives is beneficial and
incidence ofallogeneic fusion will also increase, and se- favored by selection, then the ability to exploit this in-
lection on the allele via somatic parasitism will operate formation at the time ofsettlement will also be favored.
in the opposite direction, preventing the allele from Conversely, selection for selffusion will not generate se-
reaching fixation in the population. lection forrecognition at the larval stage (except perhaps
As a consequence of frequency-dependent selection, to avoid settlement near fusible larvae and adults).
high levels ofallele polymorphism are expected in pop- Hence, allorecognition systems in botrylloid ascidians
ulations (26). In addition to preserving new alleles that and hydractiniid hydroidsdemonstrate featuresthat may
enterthe population by chance, frequency-dependent se- havebeen shapedbytheselective pressuresofboth fusion
lectionmayindirectlyincreasetherateatwhichnewalleles with kin and fusion with self. Because the aggregation of
are generated. Frequency-dependent selection could favor fusiblelarvaeisabsentinhydractiniid hydroids,thisfamily
alleles at modifier loci that generate new alleles at the appears to display mainly the effects ofselection for self
targetlocusbytwodifferent mechanisms. Modifieralleles fusion. However, data on botrylloid ascidians provide
could increase either mutation rates in the gene coding supportforbothhypotheses. Thisisnotasurprisingresult,
forallorecognition (27) or recombination rates within this as these two selective forces are not mutually exclusive
genesequence(intragenic recombination) (28). Although and their relative impact may vary among taxa. A more
frequency-dependent selection has previously been rec- rigorous evaluation ofthese two hypotheses will require
ognized asthe most likely explanation forhigh allorecog- further data on the costs, benefits, and, especially, the
nition allele diversity (1), an ecological scenario that gen- relativefrequencyofselfandkin fusion. Forthemoment,
erates frequency-dependent selection has been lacking. we suggestthatcurrentdataareatleastasconsistentwith
In the colonial ascidian Botryllus schlosseri, chimeras the selective pressuresgenerated byselffusion asthey are
formedbythefusionoftwocoloniesofdifferentgenotype
with kin selection.
(allogeneic fusion) eventually terminate in either the ab- The resolution ofthe issue ofthe selective forces op-
sthoerpttwiooncoolfooninees,coolfotennyabcyctohmepaonthieerdobrytthheesdeepaatrhatoifononoef eratingwithin allorecognition systems hasadditional im-
(29-31). Although initially noted in caseswhere the fusing pSleilceacttiioonnshoansocuormuendteorsbteanvdiienwgedofaesvoalfuotricoenatrhyatproopceersastees.s
calosloonoicecsusrhsarwehdeonnlbyotohnealallolroerceocgongintiitoinonalallelleelse,atrheissrheasrueldt onmanydifferentbiologicallevels, leadingsometosuggest
(32). This phenomenon is not restricted to ascidians; a that the major features ofbiological organization are es-
high percentage ofallogeneic chimerasofthecolonial hy- tablished during transitions in levels ofselection (8. 36).
droid Hvdractinia symbiolongicarpus are also unstable In this light, kin selection has provided ajustification for
(33). The break-up ofchimerasin this species islinked to the suggestion that allorecognition systems function to
mediate and control conflict between two different levels
the onset ofreproduction, further suggesting that recog-
nition decisionsareimpactedbythepotential forsomatic ofselection, the genotype and the colony (3). Ifselection
is found to occur predominately at the individual level,
cell parasitism (33).
The observation that most chimeras formed by kin fu- then allorecognition should be viewed in a very different
sion are unstable andtemporary isclearly notcompatible light, as a system that attempts to restrict selection to a
with a system dominated by kin selection. Few benefits single level by maintaining synonomy between genotype
are likelytobe received bytheparticipatingcoloniesdur- andcolony. A logical extension ofthisperspectivesuggests
ingashortassociation, andtheultimate resultisgenerally that new biological systems may arise not onlytoaccom-
deleterious to at least one of the participating colonies modate and organize new levels ofselection, but also to
(29-31). In fact, the negative consequences ofkin fusion hinder hierarchical expansion.
158 M. FELDGARDEN AND P. O. YUND
Acknowledgments 19. Mukai, H., and H. Watanabe. 1975. Distribution offusion in-
Wethank Leo Buss, John Francis, SteveGaines, Howie Bcoomtpraytlilbuislpirtiymtiygpeensusin.nPartoucr.alJppno.puAlcaatdi.on5s1:of4t4h-e4c7.ompoundascidian,
Lasker, Pam O'Neil, and Buki Rinkevich for comments 20. Scofield,V.L.,J. M.Schlumpberger, L.A.West,andI.L.Weiss-
on earlier versions ofthis manuscript. Financial support man. 1982. ProtochordateallorecognitioniscontrolledbyaMHC-
wasprovided by the National Science Foundation (OCE- likegenesystem. Nature295: 499-502.
89-00325 and OCE-91-96014). 21. Hauenschild, V. C. 1954. Genetische und entwichlungphysiolo-
gische Intersuchungen uber Intersexualitat und Gewebevertragli-
Literature Cited chkeit bei Hydractinia cchinata Flem. Wilhelm Roux'Arch. En-
twicklungsmech. 147: 1-41.
1. Grosberg, R.K. 1988. Theevolutionofallorecognitionspecificity 22. Hauenschild, V. C. 1956. Uberdie VererbungeinerGewebever-
inclonal invertebrates. Q. Rev. Biol. 63: 377-412. traglichkeits-eigenschaftt bei dem Hydroidpolypen Hydractinia
2. Buss, L. W.,and D. R.Green. 1985. Histoincompatibility inver- echinata. Z. Naturforsch. lib: 132-138.
3. ctBleubosrnsaa,tlesLi:.nvtWehre.terbe1rl9ai9ct0te.sh.ypTCortoehmnepsdeistsi.EtcDoileo.vnEwvCoioltm.h;i'5n.:a3In5m2dm-u3bn5e6ot.wlee9n: 1en9c1r-u2s0t1i.ng 23. YHuydnrda,ctPi.niOa.,spa.ndnovH..CM.inPtahrekeGr.ul1f9o8f9.MaiPnoep.ulJa.tiEoxnp.stMraurc.turBeiolo.f
4. Buss, L. W. 1982. Somatic cell parasitism and the evolution of Ecol. 125: 63-82.
somatictissuecompatibility.Proc.Natl.Acad.Sci. U.S.A.79:5337- 24. Crozier,R.H.1986. Geneticclonalrecognitionabilitiesinmarine
invertebrates must be maintained by selection for somethingelse.
5341.
5. Jackson, J. B. C. 1985. Distribution and ecology ofclonal and Evolution40: 1100-1101.
aclonal benthic invertebrates. Pp. 297-356 in Population Biology 25. Grosberg, R. K., andJ. F.Quinn. 1988. The evolution ofallore-
andEvolution ofClonalOrganisms. }. B. C. Jackson, L. W. Buss, cognition specificity. Pp. 157-167inInvertebrateHistorecognition.
and R. E. Cook, eds. Yale UniversityPress, New Haven, CT. R. K. Grosberg, D. Hedgecock, and K. Nelson,eds. Plenum Press,
6. Hughes,T. P.,andJ. B.C.Jackson. 1985. Population dynamics NewYork.
andlifehistoriesoffoliaceouscorals. Ecol. Monogr. 55: 141-166. 26. Ayala,F.J.,andC.A.Campbell. 1974. Frequency-dependentse-
7. Wulff,J.L. 1986. Variationinclonestructureoffragmentingcoral lection. Ann. Rev. Ecol. Sysl. 5: 115-138.
reefsponges. Biol J Linn. Soc. 27: 311-330. 27. Ohno, S. 1969. Thespontaneous mutation rate revisited and the
8. Buss,L.\V. 1987. TheEvolutionofIndividuality. PrincetonPress, possibleprincipleofpolymorphism generatingmorepolymorphism.
NJ. Can. J. Genet. Cytol. 11:457-467.
9. McFadden, C. S. 1986. Colony fission increases particle capture 28. Bodmer, W. F., and A.J. Darlington. 1969. Linkage and recom-
rates ofa soft coral: advantages ofbeing a small colony. J. E\p. binationatthemolecularlevel. Pp.223-265inGeneticOrganization.
Mar. Biol. Ecol 103: 1-20. Vol. 1. E. W. Caspari andA. W. Ravin,eds. AcademicPress, New
10. Lasker, H. 1990. Clonal propagation and populationsdynamics York.
ofagorgoniancoral. Ecology71: 1578-1589. 29. Rinkevich, B., and I. L. Weissman. 1987. A long-term study on
11. Karakashian, S., and R. Milkman. 1967. Colony fusion compat- fused subclones in the ascidian Botryllusschlossen: the resorption
ibilitytypesin BolryllussMosseri. Biol. Bull. 133:473. phenomenon(Protochordata: Tunicata).J. Zoo/(Land.)213: 717-
12. Hildemann, W. H., I. S. Johnston, and P. L. Jokiel. 1979. 733.
Immunocompetenceinthelowestmetazoanphylum:transplantation 30. Rinkevich, B., and I. L. Weissman. 1987. The fate ofBolryllus
immunity in sponges. Science204:420-422. larvaecosettledwithparentalcolonies:beneficalordeleteriouscon-
13. Jokiel,P.L.,W.H.Hildemann,andC.H.Bigger. 1982. Frequency sequences?Biol. Bull. 173: 474-488.
olaftiionntesrtcroulcotnuyregrianftthaeccseppotnagneceCaolrlyresjpeocntgiioan daisffausmae.aMsaurr.e oBifolp.op7u1-: 31. Rfionlkleovwiicnhg,cB.h,iamnedraI.Lf.orWmeaitsisomnani.n1t9h8e9.colVoanriiaaltitounniincattheeoBuottrcyolmleuss
135-139.
schlosseri. Bull. Mar. Sci. 45: 213-227.
14. Niegel,J.E.,andJ.C.Avise.1983. Clonaldiversityandpopulation 32. Weissman, I. L., and B. Rinkevich. 1990. Allorecognition histo-
structure in a reef-building coral, Acropora cervicornis: self-recog- MHC
nitionanalysisanddemographic interpretation.Evolution37:437- csoommpaattiicbiolritsytriunctaurparlo?toIcmhmourndoalt.esRpeecvies1:13is:t2h2e7r-e2l4a1t.ionshipto
453.
15. Curtis, A.S. G.,J. Kerr, and N. Knowlton. 1982. Graft rejection 33. Shenk, M. A.,and L. W. Buss. 1991. Ontogeneticchangesin fu-
insponges:geneticstructureofacceptingandrejectingpopulations. sibility in the colonial hydroid Hydractinia symbiolongicarpus. J
Transplantation 30: 362-367. Exp. Zool. 257: 80-86.
16. Neigel,J.E.,andG.P.Schmahl. 1984. Phenotypicvariationwithin 34. Grosberg, R. K., and J. F.Quinn. 1986. Thegeneticcontrol and
histocompatibility-defined clones ofmarine sponges. Science 224: consequencesofkin recognition by thelarvaeofacolonial marine
413-415. invertebrate. Nature332: 456-459.
17. Neigel, J. E., and J. C. Avise. 1985. The precision ofhistocom- 35. Yund, P.O.,C. W.Cunningham, and L. W. Buss. 1987. Recruit-
patibilityresponseinclonal recognitionintropical marinesponges. mentandpostrecruitmentinteractionsinacolonialhydroid.Ecology
Evolution39: 724-732. 68:971-982.
18. Tanaka, K., and H. Watanabe. 1973. Allogemc inhibition in a 36. Maynard Smith, J. 1988. Evolutionary progressand levelsofse-
compoundascidian,BotryllusprimigenusOka. I. Processesandfea- lection. Pp. 219-230 in EvolutionaryProgress. M. H. Nitecki, ed.
turesof"non-fusion" reaction. Cell. Immunol. 7:410-426. UniversityofChicago Press. Chicago. 1L.
