Syst. Biol. 48(2):329–351, 1999

DeŽnitions in PhylogeneticTaxonomy:Critique and Rationale

PAUL C. SERENO Department of Organismal Biologyand Anatomy, Universityof Chicago, 1027E. 57thStreet, Chicago, Illinois 60637, USA; E-mail: dinosaur@uchicago.edu

Abstract.—Ageneralrationale for the formulation andplacement of taxonomic deŽnitions in phy- logenetic taxonomyis proposed, andcommonly used terms such as“crown taxon”or “ node-based deŽnition” are more precisely deŽned. In the formulation of phylogenetic deŽnitions, nested refer- ence taxastabilize taxonomic content. AdeŽnitional conŽguration termed a node-stem triplet also stabilizes the relationship between the trio oftaxa at abranchpoint,in the face oflocal changein phylogenetic relationships oraddition/ deletion of taxa.Crown-total taxonomiesuse survivorship asa criterion forplacement ofnode-stem triplets within ataxonomic hierarchy.Diversity,morphol- ogy,andtradition alsoconstitute heuristic criteria forplacement of node-stem triplets. [Content; crown; deŽnition; node;phylogeny; stability; stem; taxonomy.]

Doesone type ofphylogenetic deŽnition Mostphylogenetic deŽnitions have been (apomorphy,node,stem) stabilize the taxo- constructedin the systematicliterature since nomiccontent of a taxonmore than another then withoutexplanation or justiŽ cation for in the face oflocal change ofrelationships? the particulartype ofdeŽ nition used. The Isone type ofphylogenetic deŽnition more justiŽcation given forpreferential use of suitablefor clades with unresolved basalre- node- andstem-based deŽ nitions for crown lationshipsor uncertain outgroups? Which andtotal taxa, respectively ,isincomplete or type ofphylogenetic deŽnition is preferable inaccurate,as reviewed below. forclades whose members areentirely living Totaltaxa and crown taxarequire stem- or extinct? basedand node-based deŽ nitions, respectively. — Questionslike these havenot been rigor- Given thata totaltaxon includes allcur- ouslyaddressed in phylogenetic taxonomy. rently knownand potential extinct out- Rather,attention has been focusedon (1) the groupsthat are most closely related to a adaptationof traditionalrules governing particularcrown taxon (T able 1),the total synonymyand redundancy foruse within taxonmust have a stem-baseddeŽ nition the phylogenetic system,and (2) the recom- (de Queirozand Gauthier, 1992). The stem- mendationthat “ widely recognized”names basedstructure of the deŽnition ensures the arebetter restrictedto crown taxa than to inclusionof all taxa up to,but excluding, the more-inclusive taxawith extinct basal mem- commonancestor shared with its sister to- bers (de Queirozand Gauthier, 1990, 1992; taltaxon. This justiŽ cation is sufŽ cient, be- Roweand Gauthier ,1992;Bryant, 1994, 1996; causeneither anapomorphy- nor a node- Lee, 1996).Despite increasinguse ofphy- baseddeŽ nition would include allpotential logenetic deŽnitions in systematics,a gen- extinctoutgroups. eralrationale has yet tobe proposedfor Acrowntaxon, in contrast,does not the formulationand placement ofphyloge- require anode-based deŽnition, although netic deŽnitions, and manycommonly used one iscommonly assumed. De Queiroz termssuch as “ crowntaxon” and “ node- andGauthier (1992:469) simply remarked, baseddeŽ nition” have yet tobe speciŽcally “Namescan be associatedunambiguously deŽned. withcrown clades using node-based def- initions.”Likewise, Roweand Gauthier (1992)and McKenna andBell (1997)pro- LACK OF A GENERAL RATIONALE posednode-based deŽnitions for Mammalia DeQueirozand Gauthier(1990, 1992) Ž rst withoutexplaining why deŽnitional type articulatedthe general structureof phylo- ispreferable. Lee (1996:1103)remarked, “ A genetic deŽnitions, outlining apomorphy-, crown-cladedeŽ nition results when both node-, andstem-based deŽ nitions (Fig. 1). taxaimplicated in anode-based deŽnition

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deŽnition will moreeffectively stabilizetax- onomiccontent. Thus, there isno current justiŽcation for exclusive use ofnode-based deŽnitions to delimit crown taxa. Node- basedcrown taxa, in conjunctionwith stem- basedtotal taxa, however, yield alocaldef- initionalconŽ guration that can provide jus- tiŽcation for preferential use ofnode-based crowntaxa (see Node-Stem Triplet below). Node-basedcrown taxaare more stable,infor- mative,and accurate thantaxa deŽ ned by ex- tinct speciesand have been (or shouldbe) as- FIGURE 1.Node-based and stem-based phyloge- sociatedwith “ widelyused” names. —Gauthier netic deŽnitions, which usually havebeen shown (1986:12)stated that restricting “ Aves”to graphicallyby encircling portions of acladogram(de Queiroz andGauthier, 1992), are indicated here byadot “living taxa”maximizes “ stabilityand phy- (node-based)or arrow (stem-based). logenetic informativeness,”and de Queiroz andGauthier (1992:468) suggested that“ bi- ologistscommonly use the widely known arerepresented by extantforms.” And Wyss nameA veswhen makinggeneralizations andMeng (1996:559)stated that the deŽni- thatapply toextant birds alone.” With re- tionsof crown taxa “ arethus node-based in gardto the taxonMammalia, Rowe and their formulation,”without presenting any Gauthier(1992:372) observed that “ noone reasoningfor such a conclusion. in severalcenturies hasmistakenly assigned Any group of extantspecies mayjust aRecentmammal to some other taxon.” aswell be united by astem-baseddeŽ ni- McKenna andBell (1997:32)remarked that tion.The crowntaxon Amniota, for example, “acrowngroup islikely toremain relatively couldhave a stem-baseddeŽ nition, such as: stable.” “anyRecent tetrapod more closely related to Despite these andsimilar statements in Mammaliathan to Anura and all extinct de- the literature,node- orstem-based crown scendantsof their mostrecent commonan- taxaare not demonstrably more stable in cestor.”A stem-baseddeŽ nition for a crown terms of meaning or content.Any node- or taxon,in fact,may be preferable if the basal stem-baseddeŽ nition that speciŽ cally iden- relationshipsamong extant taxa within a tiŽes a mostrecent commonancestor clearly crownclade are poorly established, as seems speciŽes the boundariesof a clade,regard- tobe the casewith Amniota (see alsoRo- lessof the living orextinct status of the ref- dentia:Wyss and Meng, 1996)(Fig. 2b).All erence taxaor the particularphylogeny to members ofthe crowntaxon will be in- whichthe deŽnition is applied (Lee, 1996). cluded, even if basalingroup relationships In termsof taxonomic content, redeŽ n- arepoorly resolved, because astem-based ing Mammaliaas a crowntaxon does not deŽnition is based on reference toan out- immediatelyclarify which extinct taxa will group taxon(or taxa). be included orexcluded. Mammaliaas Asingle suboscinebird, for example, acrowntaxon appears more stable only wouldsufŽ ce asan outgroup reference if extincttaxa are ignored andattention taxonfor a stem-baseddeŽ nition of the isfocused on the greatphylogenetic dis- crowntaxon Oscines. A node-based deŽ- tanceto their nearest living sistergroup. nitionof the samecrown taxon would re- Even so,inclusion of someliving mam- quire listingmany oscine subgroups toen- malsmay be uncertain.Rowe and Gau- sure inclusionof all living species currently thier’s(1992:375)preferred node-based def- regardedas oscines. On the otherhand, if initionof Mammalia (“ the lastcommon the basaldichotomy within a crowntaxon ancestorof Monotremata and Theria” ; see iswell establishedand outgroup relation- alsoMcKenna andBell, 1997:32,35.)may shipsare uncertain (Fig. 2a),a node-based be synonymouswith Theria, if monotremes 1999 SERENO—RATIONALE FOR PHYLOGENETICDEFINITIONS 331

TABLE 1.DeŽ nitions forterms used in this paper.

Term DeŽnition TaxonomicdeŽ nition relational statement specifying the taxonomic content of ataxon Taxonomicdiagnosis descriptive statement specifying the apomorphies (derived characterstates) thatserve to identify membersof ataxon Taxonomiccontent existing andpotential taxaor individuals thatby deŽnition areincluded within ataxon Reference taxon taxonserving asareference in aphylogenetic deŽnition Crown taxon aliving species, ora clade thatcan be deŽned by living species, whose immediate outgroup is extinct Total taxon clade composed of acrown taxonplus all extinct outgroups more closely related to it thanto anothercrown clade Stem taxon anextinct species orclade forwhich immediate outgroup includes atleast oneliving member Node-baseddeŽ nition statement specifying aclade composed of the most recent commonancestor of two ormore reference taxaand all descendants Stem-baseddeŽ nition statement specifying aclade composed of all descendantsmore closely related to onereference taxon(or taxa) than another (or others) ComplementarydeŽ nitions phylogenetic deŽnitions with the samereference taxa(as in anode-stem triplet) Reciprocal deŽnitions phylogenetic deŽnitions with the samereference taxabut in reverse order (asin opposing stem-basedtaxa of anode-stem triplet) Node-stemtriplet trio of taxawith complementary deŽnitions consisting of anode-based taxonand two subordinatestem-based taxa Taxonomicequivalence statement of equivalence (orequation) in which the taxonomic content of onetaxon equals that of subordinatetaxa plus their commonancestor (e.g.,A =B+C,asin anode-stem triplet) proveto be moreclosely related to marsu- thanto suppose thatthe ancientbird hadthis pials,as indicated by somerecent molecu- sequence (Lee, 1996).Accelerated character- larevidence (Penny andHasegawa, 1997). statetransformation, in otherwords, is not Stabilityof taxonomiccontent is not re- morecorrect, accurate, or informative than latedto the living orextinct status of ref- delayed transformation. erence taxain aphylogenetic deŽnition, Historicaland current usage, such as may but ratherto the particularchoice of ref- be ascertained,also does not clearly asso- erence taxa.For many node-based deŽni- ciate“ widely used”names with crown taxa tionsof crown taxa, stability is also re- (Bryant,1994; Lee, 1996).Regarding Mam- latedto the certaintywith which aspeciŽed malia,Rowe and Gauthier (1992:375– 376) basaldichotomy has been correctlyascer- statedthat “ itsuniversal usage by compar- tained. ativebiologists, except forsome paleontol- That“ widely used”names, such as Aves, ogists,has long been forthe crownclade shouldbe assignedto crown taxa has been Mammals,viz., the lastcommon ancestor of justiŽed by arguing that(1) neontologists Monotremataand Theria, and all of its de- shouldreport their observationsaccurately , scendants,”and that “ currentdebate over referring only tocrown clades rather than the nameMammalia highlights the factthat crownclades plus someof their extinctout- manypaleontologists continue tooperate in groups,and that (2) doing sofollowslong- asystemin uenced in fundamentalways by standingtaxonomic practice (de Queiroz apre-Darwinian worldview.” Darwin was andGauthier, 1992). The conditionin ex- fairly clearregarding hisconception of the tinctoutgroups for characters that are not taxonomiccontent of Aves,Mammalia, Mar- preserved, however,is ambiguous. T osup- supialia,and othergroups with living repre- pose that Archaeopteryx lackedan apomor- sentatives.For Darwin, these taxaincluded phic molecularsequence found in crown- fossilstem groups. In TheOriginof the Species group birds(Neornithes) isno more justiŽ ed (1859:268),he wrote: 332 SYSTEMATICBIOLOGY VOL. 48

placentata,or Marsupials; not, however, fromforms closely resembling the existing Marsupials,but from their earlyprogenitors. Mostextant biologists also conceive ofthe taxonomiccontent of Mammalia in asimi- larfashion, whether they areevolutionary taxonomists,cladists, ecologists, or molec- ularbiologists (e.g., Jollie, 1973:76–77; Fu- tuyma,1986:334; W alker,1975).Higher taxa suchas Mammaliaand A veshave been asso- ciatedwith “ key”characters and their asso- ciatedfunctions. Archaeopteryx ,withfeath- ers,wings, and the capacityfor  ight,will alwaysbe considereda “bird”within A ves by the majorityof biologists. Altering this equationfor well-established monophyletic taxais likely toengender confusion. Stem-based deŽnitions are less “ consistent” thannode-based deŽ nitions. —Schander and Thollesson(1995:264) suggested thatstem- baseddeŽ nitions “ refer tonon-existing cladesunder somephylogenetic resolu- tions.”They presented anexample (Fig. 3a) in whichrelocation of one taxon(taxon A) resultsin adeŽnition that refers toan “im- possible”clade. Relocation of taxon A cre- atesthis internal inconsistency because the originalingroup reference taxon(taxon F) forstem-based taxon G nowincludes by def- initionthe originaloutgroup taxon (taxon

FIGURE 2.Crown taxa, deŽ nitional types, andsta- D).Schander andThollesson(1995:264) con- bility.(a)A crown clade with resolved basalrelation- cluded that“ if aconsistentsystem of taxon- ships but with unresolved outgroup relationships may omyis wanted, stem-based deŽ nitions may bedeŽned with greatest stability asanode-basedtaxon. better beavoided.” (b)A crown clade with unresolved basalrelationships Similarinternal “ inconsistency,”how- but with astable extinct outgroup maybe deŽned with ever, canbe generated fornode-based taxa greatest stability asa stem-basedtaxon. Crown groups areencircled; dashedlines indicate extinct taxa;a dot aswell (Fig. 3b).In thisexample, relocation indicates anode-baseddeŽ nition; anarrowindicates a ofone taxon(taxon A) resultsin adeŽnition stem-baseddeŽ nition. thatrefers toan “impossible,”or internally redundant,clade. Relocation of taxon A cre- atesthis internal inconsistency ,because one those groupswhich have,in knowngeological pe- ofthe originalreference taxa(taxon E) for riods,undergone much modiŽcation, should in the node-based taxonG nowincludes the other older formationsmake some slight approachto each reference taxon(taxon F) andthe common other;so that the older membersshould differ less in ancestor.Even if taxonE isregarded as aju- some of their charactersthan do the existing mem- bersof the samegroups. niorsynonym of taxon G afterrelocation of taxonA, the deŽnition of taxonG mustbe About mammals,Darwin (1859:522) wrote: changed (because taxonE cannotbe used as areference taxon). They[marsupials] appeared in anearlier geological period, andtheir rangewas formerly much moreex- Ratherthan demonstrating any partic- tensive thanat present. Hence the Placentataare gen- ularstructural weakness of stem-based erally supposed to havebeen derived fromthe Im- deŽnitions, these examples(Fig. 3)better 1999 SERENO—RATIONALE FOR PHYLOGENETICDEFINITIONS 333

descendants”; taxonE is deŽned as “ taxonA, taxonB, their commonancestor, and all descendants”;and taxon Fis node-basedand deŽ ned as “taxonC, taxonD, their commonancestor, and all descendants.”Taxon G is “in- consistent”after relocation oftaxon A, because one of its reference taxa(taxon E) now includes bydeŽnition the other reference taxon(taxon F) andthe common ancestor.The reference taxafor a node-basedtaxon are presumed to beexclusive ofone another and their com- monancestor; after relocation oftaxon A, these condi- tions areviolated fortaxon G asoriginally deŽned. The “inconsistency,”however, disappearsif aless-inclusive reference taxonhad originally beenselected fortaxon G (i.e.,taxon A orB ratherthan taxon E). Inthis case,taxon Gexists afterrelocation of taxonA (either unchangedin its taxonomic content, oras aless-inclusive taxonthat excludes taxonB, dependingon whether taxonB orA wasused asan ingroup reference taxon,respectively). Dots indicate node-baseddeŽ nitions, andarrows indi- cate stem-baseddeŽ nitions.

illustrateproblems that arise asa resultof se- lecting maximallyinclusive reference taxa— the mostcommon kind ofreference taxa currently chosenin phylogenetic deŽnitions (see Reference Taxa below). If Schander and Thollessonhad chosen a morenested in- group reference taxonin their stem-based deŽnition of taxon G (i.e., taxonA orB rather thantaxon F; Fig. 3a),relocation of taxon Aposesno special problems. In thiscase, taxonG either refers tothe sameclade mi- FIGURE 3.Problems associated with maximallyin- nus taxonA (if taxonB isthe ingroup ref- clusive reference taxa.(a) Relocation of taxonA results erence taxon)or becomesa potentialjunior in an“ inconsistent”stem-based deŽ nition fortaxon G, because itdeŽnes agroupthat cannot exist underthe al- synonymof taxon A (if taxonA isthe in- ternative phylogenetic hypothesis (afterSchander and group reference taxon).Similarly ,fornode- Thollesson, 1995:Fig.3). Schander and Thollesson de- basedtaxon G (Fig. 3b),a morenested refer- Žnedstem-based taxon G as“Fandall taxasharing a ence taxon(taxon A orB ratherthan taxon more recent commonancestor with it thanwith D,”and E)removesany inconsistency after reloca- stem-basedtaxon F as“ Aandall taxasharing a more tionof taxon A. TaxonG refers either tothe recent commonancestor with it thanwith C.”Taxon sameclade (if taxonB isan ingroup refer- Gis “inconsistent”after relocation of taxonA, because ence taxon)or to a lessinclusive cladethat its ingroup reference taxon(taxon F) now includes by deŽnition the outgroup reference taxon(taxon D). The excludes taxonB (if taxonA isan ingroup “inconsistency,”however, disappearsif aless-inclusive reference taxon). ingroup reference taxonhad been chosen fortaxon G Node-or stem-based deŽnitions better re- (i.e.,taxon A orB ratherthan taxon F). Inthis case, ect originalusage and content. —Gauthier taxonG exists afterrelocation of taxonA (either asa (1986:12,13), for example, suggested thathis synonymof taxonA, oras a groupincluding taxaB stem-baseddeŽ nition for Haeckel’ s (1866) andC, dependingon whether taxonA orB was used as taxonOrnithurae (“ Extantbirds and all the ingroup reference taxon,respectively). (b)Reloca- tion oftaxon A results in an“ inconsistent”node-based othertaxa, such as Ichthyornis and Hes- deŽnition fortaxon G, because it deŽnes agroupthat perornithes[sic], that are closer to extant cannotexist underthe alternativephylogenetichypoth- birdsthan is Archaeopteryx ”)was“ in keep- esis. Inthis example, taxonG is node-basedand deŽned ing withits original intent” (Fig. 4).Chiappe as“ taxonE, taxonF ,their commonancestor, and all (1991,1996), on the otherhand, argued that 334 SYSTEMATICBIOLOGY VOL. 48

Ornithuraeis better deŽned asalessinclu- rae,as noted by Gauthier(1986), has been sivenode-based taxon,with Hesperornithi- supplanted by Neornithes(Gadow ,1893), formesand Neornithes (crown-group birds) ataxonreferring tocrown-group avians. asreference taxa(Fig. 4).Initially ,Chiappe Basedon original intent, an argument could be madethat Haeckel’ s Ornithuraeshould supplantNeornithes on grounds of prior- ity,orthat it be deŽned explicitly asan apomorphy-basedtaxon based on the pres- ence ofapygostyle, which isnow known to be lacking in birdsother than Archaeopteryx (Forsteret al.,1998). In either case,the deŽnition would circumscribe clades other thanthose identiŽ ed by either Gauthieror Chiappe. Formost taxon names, the originaldeŽ - nition,if explicitly statedat all,is character- basedor taxon-based (a list of included taxa) andlacks a relationalphrase about ances- trythat would specify potential membership. The intent ofthe originalauthor of a taxon toinclude orexclude unknown, orreposi- FIGURE 4.Cladogram of basalavians showing re- cent use of the highertaxon Ornithurae (Haeckel,1866). tioned,taxa usually cannotbe interpreted Thedot indicates anode-baseddeŽ nition, andthe ar- unambiguously.Thisproblem isnot widely row indicates astem-baseddeŽ nition. appreciated.

(1991:337)reasoned that a node-based deŽ- APOMORPHY-BASED DEFINITIONS nitionof Ornithurae was more appropriate An apomorphy-baseddeŽ nition speci- because itexcluded severalnewly discov- Žes the boundariesof a cladeby identi- ered basalavians that lacked some of the fying the “Žrstancestor with a particular synapomorphiesin Gauthier’s(1986)diag- synapomorphy”(de Queirozand Gauthier, nosisof Ornithurae. Later Chiappe argued 1990:310)and encompassing all of its de- thata node-based deŽnition of Ornithurae scendants.An apomorphy-basedtaxon in- “better reects the compositionof the clade cludes alldescendants, whether ornot the before to[sic] the applicationof phyloge- synapomorphyis maintained. Apomorphy- netic deŽnitions” (1996:205). baseddeŽ nitions are subject tothree prob- Neither Gauthier’snorChiappe’ s deŽni- lemsthat are not relevant to node-based and tionshave historical precedence. Haeckel stem-baseddeŽ nitions: variation in charac- (1866)coined Ornithurae (“ bird tail”) forthe tercoding, optimization ambiguity ,andho- reduced number ofvertebrae andunique moplasy(Bryant, 1994; Schander andThol- coossiŽcation of the distaltail (as a sin- lesson,1995; Sereno, 1998).These problems gle bone, the pygostyle) thatcharacterizes havelong been associatedwith traditional allextant birds, in contrastto the condi- use of“ key”characters to deŽ ne taxa.Thus tion in Archaeopteryx .Haeckel’s taxonowes far,few apomorphy-baseddeŽ nitions have itsexistence tothe then-recent discoveryof been erected, andthis deŽ nitional form Archaeopteryx ,aprimitivebird witha tail shouldbe avoided. comprisingover 20 vertebrae. Contrary to Characterambiguity. —Consideran apo- Chiappe (1996),Ornithurae predates the de- morphy-based deŽnition for A ves(includ- scriptionof the extinctshort-tailed genera ing Archaeopteryx andOrnithurae) based on Hesperornis (Marsh,1872a) and Ichthyor- the presence of“ feathers,”the “key char- nis (Marsh,1872b) or the taxonHesper- acter”usually associatedwith this taxon. ornithiformes(F urbringer,¨ 1888).Ornithu- First,the charactercoding— “Feathers: ab- 1999 SERENO—RATIONALE FOR PHYLOGENETICDEFINITIONS 335 sent(0); present (1)”— isonly one ofsev- animpasse for an apomorphy-baseddeŽ ni- eralpossibilities. A “feather”iscomposed tion,because the apomorphymight identify ofa rachis,barbs, barbules, andother com- morethan one clade.Invoking timeas an ar- ponentsthat may be better codedas sepa- biter (such as“ the Žrsttaxon that has . . .”) ratecharacters. The characteron which an invitesambiguities associated with tempo- apomorphy-baseddeŽ nition is based, there- ralorigin (such asmissing ancestral lin- fore,may be recodedas two or more char- eages). acterswith independent character-statedis- tributions.Indeed, thisis an expectation for mostqualitative or quantitative characters; PHYLOGENETIC DEFINITIONS: TERMINOLOGY thatis, once the transformationsbecome bet- The terminologyused in the following terknown, intermediate states or multiple discussionof phylogenetic taxonomicdef- characterswill emerge, asrecent discoveries initionsis clariŽ ed below andtabulated (T a- arebeginning toreveal with regard to feath- bles 1,2).Some ofthesetermsare given more ers(Chen etal., 1998; Ji etal., 1998), or with speciŽc meaning thanin the currentlitera- regardto the charactershistorically associ- ture;others are new orrecently introduced atedwith Mammalia (Rowe, 1988; Rowe and (Sereno, 1998). Gauthier,1992; Bryant, 1994; de Queiroz, TaxonomicdeŽ nition and diagnosis are de- 1994). Žned here muchasthey havebeen described Theapomorphy-baseddeŽ nition given as previously byphylogenetic systematists(de anexample by de Queirozand Gauthier Queirozand Gauthier ,1990,1992) and their (1990:310)is subject onthe samegrounds forebears(Buck andHull, 1966;Farris, 1976; tointerpretational ambiguity: “ Tetrapoda” Ghiselin,1984) (T able 1).De Queirozand isdeŽ ned asthe “Žrstvertebrate to possess Gauthier(1992:461) deŽ ned phylogenetic digits(i.e., handsand feet ratherthan Ž ns) deŽnitions as “ statementsspecifying the andall of its descendants.” What exactly meaningsof taxon names (words); they are constitutesa “digit”versus a “Žn”or “ pad- statedin termsof ancestry .”The “meaning dle”? In fact,this is a signiŽcant question ofa taxonname” in phylogenetic taxonomy given recent fossildiscoveries (Daeschler concernsits taxonomic content, or mem- andShubin, 1998).Can this feature, orlist bership, asdelimited by arelationalstate- offeatures, be observedin extinctforms? ment.T axonomicdeŽ nitions, therefore, are And whathappens if welearnthat “ digits” regardedhere as“ extensional”(ostensive) evolved Žrston the handsand later on the statementsof relationship that specify the feet? These arecommon problems in the in- taxonomiccontent of a taxon(de Queiroz, terpretationof character data, which should 1992). notbe extended totaxonomic deŽ nitions. Taxonomicdiagnosis, on the otherhand, Optimizationambiguity. —Apomorphy- involvesthe “intensional”characterization baseddeŽ nitions also do not specify asin- ofmembers ofa clade,as recognized by gle ancestorwhen the chosenapomorphy the sharedapomorphies present in the hasan ambiguous optimization. Charac- commonancestor (Buck andHull, 1966; terswith ambiguous character-state opti- Farris,1976; Ghiselin, 1984; Rowe, 1987; mizationare commonplace in systematics de Queirozand Gauthier, 1990, 1992; de andarise from missing data (lack of preser- Queiroz,1992). According to de Queirozand vation,strong transformation) and homo- Gauthier(1992:461), diagnoses are “ state- plasy(Bryant, 1994; Schander andThol- mentsspecifying howto determine whether lesson,1995; Sereno, 1998).There maybe agiven species ororganism is a representa- manyequally parsimoniouspositions for tiveof the taxon(clade) towhich apartic- aparticularcharacter state on the shortest ularname refers; they aremost commonly cladogram. statedin termsof characters.” Strictly speak- Homoplasy.—Homoplasymay involve the ing, sharedapomorphies (derived-character stableplacement ofan apomorphyat more states),rather than characters, determine the thanone node (Bryant,1994). This can create membership ofa particularclade or species. 336 SYSTEMATICBIOLOGY VOL. 48

Taxonomiccontent isused here torefer to (Schander andThollesson, 1995), these all existing and potential taxaincluded by the importantcomponents of phylogenetic phylogenetic deŽnition of a taxon(T able 1). deŽnitions have not been distinguished The smallestnumber ofsubordinate taxa terminologically. thatcan fulŽ ll thisdeŽ nition of taxonomic Several kinds ofreference taxacan be contentis two; a redundanttaxon (i.e., a identiŽed (Fig. 5;Table 2). Ingroup and out- single subordinatetaxon) would have an group reference taxaare located within or identicalphylogenetic deŽnition and, thus, outsidethe taxonthey deŽne, respectively isuninformative in phylogenetic taxonomy (Fig. 5a,b). An inclusive reference taxonin- (Farris,1976). The taxonomiccontent of cludes severalingroup oroutgroup taxa; taxonC, therefore, couldbe “taxonA, taxon amaximallyinclusive reference taxonin- B,their mostrecent commonancestor, and cludes the largestpossible ingroup orout- alldescendants,” if taxaA andB aredeŽ ned group reference taxon(Fig. 5c).Basal and extensionallyto encompass all existing and nested reference taxaare less inclusive and, potentialsubordinate taxa currently within astheir namesuggests, are located at the taxon C. baseor nested withinan ingroup orout- Alistof included taxais insufŽ cient toun- group taxon(Fig. 5d,e). ambiguouslyspecify taxonomiccontent, be- A crown taxon denotesa living species, causethere will alwaysbe potentialmem- ora cladedeŽ ned by using living refer- bers ofa taxonthat lie outsideany list of ence taxa,whose immediate outgroup is included taxa,whether ornot the included extinct(Figs. 6,7; Table 1).The extinctout- taxathemselves have phylogenetic deŽni- group isa necessarycomponent of the def- tions.An exhaustivelist of included taxa inition.Jefferies (1979:449)coined the term withstem-based deŽ nitions, for example, “crowngroup” to replace Hennig’s (1969) doesnot specify membership fortheir hy- *group, whichJefferies deŽned as“ the lat- potheticalimmediate common ancestor (a estcommon ancestor of all living members node-based taxon)or more distant known ofgroup 1,plus alldescendants of this an- orhypothetical outgroups (a stem-based cestor,whether these areliving orextinct.” taxon).T woreference taxaand a relational Theexistence ofan immediateoutgroup that statementabout ancestry are necessary and isextinct is implied andwas clearly present sufŽcient tospecify taxonomiccontent, be- in the examplesgiven by Hennig andJef- causethey unambiguously specify member- feries. Patterson(1981:207) also clearly used ship forall existing and potential members crown-and stem-groups in thismanner, of a taxon. statingthat the “stem-group containsfos- A reference taxon isa species orhigher-level siltaxa that exhibit some,but notall of the taxonthat is used todelimit a phylogenetic charactersof the crown-group.”Crown- and deŽnition (Table 1).For example, “taxonA, stem-group terminologyhas been used ex- taxonB, their mostrecent commonancestor, clusively forhigher taxabounded by liv- andall descendants” uses A andB asrefer- ing species thathave extinct outgroups (e.g., ence taxafor a node-based taxonomicdeŽ ni- deQueirozand Gauthier ,1992;Forey ,1992; tion.Previously citedas “ reference points” McKenna andBell, 1997).Although itmay

TABLE 2.DeŽ nitions forthe various kindsof reference taxa.

Reference taxontype DeŽnition

Ingroup reference taxonincluded within ataxonby deŽ nition Outgroup reference taxonexcluded froma taxonby deŽnition Inclusive most inclusive reference taxonamong ingroup oroutgroup taxa Basal reference taxonnear the basalfurcation of ataxon Nested reference taxondistant fromthe basalfurcation of ataxon Vernacular vernacular nameused asareference taxon(e.g., “ birds”or “ extantbirds” ) 1999 SERENO—RATIONALE FOR PHYLOGENETICDEFINITIONS 337

FIGURE 5.Kinds ofreference taxa.(a) An ingroup reference taxonis included bydeŽnition within ataxon;a node-baseddeŽ nition is basedon two ingroup reference taxa.(b) An outgroup reference taxonis excluded by deŽnition froma taxon;a stem-baseddeŽ nition is basedon one ingroup andone outgroup reference taxon.(c) An inclusive reference taxonis the most inclusive ingroup oroutgroup reference taxonpossible; inclusive reference taxaB andC fortaxon A allow deŽnitional ambiguitywith changein the relationship of abasaltaxon. (d) A basalreference taxonis located at,or near, the baseof aningroup oroutgroup taxon;basal reference taxaallow deŽnitional ambiguitywhen their relationships change.(e) Anested reference taxonis remote fromthe baseof aningroup oroutgroup reference taxon;nested reference taxaare unaffected bychangesin the relationships of basaltaxa. Reference taxaare encircled; adot indicates anode-baseddeŽ nition; anarrowindicates astem-based deŽnition; adashedline indicates achangein position of abasaltaxon.

FIGURE 6.Crown, stem, andtotal taxa.(a) T otal groupcomposed of acrown groupplus aparaphyletic “stem group,”as conceived byHennig (1969, 1983) and Jefferies (1979).(b) Total taxon composed of acrown taxonand monophyletic stem taxa,as used in this article. One stem taxon(left) is shown with anode-baseddeŽ nition and the other (right) with astem-baseddeŽ nition. 338 SYSTEMATICBIOLOGY VOL. 48

ing representatives.De Queirozand Gau- thier (1992:469)deŽ ned crowntaxa as “cladeswithin which both branches of the basaldichotomy are represented by extantdescendants,” without mention of the conditionof the immediateoutgroup. Yet,all of their examplesof crown clades haveimmediate outgroups that are ex- tinct.Regarding their craniatetaxonomy , they statedthat each stem-based taxon is composedof a “crowntaxon plus allex- tincttaxa more closely related to it than toany other crown clade” (de Queiroz andGauthier, 1992:475). Lee (1996:1103) proposedthat “ acrownclade deŽ nition resultswhen bothtaxa implicated in a node-based deŽnition . . . arerepresented by extantforms.” Although the condition ofthe immediateoutgroup is never men- tioned,Lee (1996:1103)stated that crown taxondeŽ nitions apply toclades that consistof “the mostrecent commonan- cestor of all extantforms, and all its de- scendants”(emphasis added). The pres- ence ofan immediate extinct outgroup is implied. The deŽnition of a crowntaxon presented FIGURE 7.Crown species orclades (enclosed) must havean extinct (stem) taxon(dashed) as an immediate here, in contrast,does not specify ingroup outgroup.(a) Crown species andcrown clades arede- structure(such asthe presence orabsence limited bythe presence of animmediate outgroup that ofa basaldichotomy) or deŽ nitional type is extinct. (b)Often referred to as“extant”taxa, crown (node- orstem-based) and explicitly states taxamay be composed primarily ofextinct taxa.“ Liv- thatthe immediateoutgroup(s) isextinct ing”and “ extinct”conditions aretreated asif theycon- (Fig. 7a;T able 1).Crown taxa, so deŽ ned, stitute plesiomorphic andapomorphic characterstates, canbe mapped unerringly ona cladogram respectively,of anirreversible character“ state of be- ing.”Crown clades, underthis conceptualization, are if (1) “living”and “ extinct”conditions are plesiomorphy-basedtaxa bounded by two living taxa treatedas primitive andderived character- forwhich the immediate outgroup is extinct. states,respectively ,ofthe character“ current stateof being,” and (2) if thischaracter is regardedas irreversible (i.e., Camin–Sokal be hypotheticallytrue that“ every Recent parsimony).The living state,in otherwords, group, whateverits position in thehierarchy, isalways regarded as plesiomorphic. The maybe expected tohave had a stem-group” irreversible statusof the character(state of (Patterson,1981:207), clades bounded by liv- being) isimportant, because itidentiŽ es ing taxawith immediate outgroups that are crowngroups on cladograms of living and alsoliving havenot been consideredcrown extincttaxa that would have an ambigu- taxa. ousstatus if character-statereversal were Some recent deŽnitions of crown taxa, allowed(Fig. 7b).This character-state con- however,have set aside Hennig’ s and ceptualizationof the deŽnition of a crown Jefferies’formulations as well asgeneral group capturesthe essence ofcrown taxa, usagein the literature.A lessrestric- whichhave always been used torefer to tivemeaning hasbeen proposedbased maximallyinclusive taxadeŽ ned by extant solelyon reference taxathat include liv- representatives,not simply any“ extant- 1999 SERENO—RATIONALE FOR PHYLOGENETICDEFINITIONS 339 bounded”taxon. Discovery of extinct sister closer[sic] relatedto one subgroup among taxaprovides the opportunityto recognize recent animalsthan to another ”(translated crown taxa. fromthe German;Ax, 1987:224). Jefferies Crowntaxa are often regardedas clades (1979)clariŽ ed the termto include allex- thatare bounded uniquely by living in- tinctoutgroups of a crowntaxon (Fig. 6a). groups.The use ofliving reference taxa, Otherauthors have developed moreconvo- however,is most often anarbitrary deci- luted deŽnitions that approximate the same sion.Any extinctingroup taxonthat is most end.Wiley (1981:217),for example, deŽned a closelyrelated to a living reference taxon “stemgroup” as “allfossil species ofa group couldbe used todelimit the sameclade moreprimitive thanthe mostprimitive Re- (Fig. 7b).A crownclade is deŽ ned uniquely centspecies ofthe samegroup.” These by living reference taxaonly when suchtaxa “stemgroups” are paraphyletic and often donot have extinct sister taxa (Fig. 7b),a circumscribethe same“ ancestralgroups” factthat is not widely appreciated.Crown and“ evolutionarygrades” that have mud- taxa,in otherwords, do not have any spe- died phylogenetic thinking since Darwin. cialbiological signiŽ cance beyond signal- Only afew cladistscontinue toendorse such ing thatparticular reference taxahave sur- concepts(Smith, 1994).Ax (1987:224) pro- vived toan arbitrary datum (the Recent). poseda cumbersomesolution to the prob- Informalreference tocrown taxa as “living” lem ofparaphyletic “ stemgroups” by divid- or“ extant”taxa, therefore, canbe mislead- ing theminto ancestral “ stemlineages” and ing, because acrowntaxon may be com- “representativesof the stemlineage.” The posedpredominantly of extinct species, as latterare monophyletic taxa most simply re- isthe casewith the crowntaxon Crocodylia ferred toas stem taxa. (Fig. 7b;Brochu, 1997). “ Extantcrocodil- A total taxon isregarded here asa clade ians,”if takenliterally ,refers toa small composedof acrowntaxon plus allex- paraphyleticsubset of Crocodylia. Explicit tinctoutgroups more closely related to it reference to“ crowncrocodilians” or sim- thanto another crown taxon (Fig. 3;Ta- ply “Crocodylia”is preferable touse ofthe ble 1).Hennig’ s (1969)and Jefferies’ (1979) terms“ living”or “ extant.” formulationsof the conceptare wordy but Aliving taxonis also essential to delimit similarin effect, because they restrictedin- amaximallyinclusive cladethat is entirely clusionof extinct outgroups to those most extinct—a stem taxon,ashere deŽned. A closelyrelated to a particularcrown taxon. stemtaxon denotes an extinct species or De Queirozand Gauthier(1992:470) deŽ ned clade,the immediateoutgroup of which in- atotalclade as a “moreinclusive cladecon- cludes atleastone living member (Fig. 6b). sistingof the crownclade plus itsextinct out- Many extincttaxa are not stem taxa, because groups.”This deŽ nition is incomplete, be- their immediateoutgroup is itself extinct. causeit does not specify which extinctout- Such extincttaxa are members ofmore in- groupsare included. Atotaltaxon explicitly clusive stemtaxa. Stem taxacan have either includes only thoseextinct outgroups most node- orstem-based deŽ nitions (Fig. 6b). closelyrelated to a particularcrown taxon. Stem taxaand their associatedless inclusive Node-based and stem-based deŽnitions are crowntaxon make up the taxonomiccontent constructedby (1) identifying reference taxa oftheir respective totaltaxon. and(2) attachingto them a relationalphrase Stem taxa,as here deŽned, shouldnot thateither includes their mostrecent com- be confused with“ stemgroup” (Fig. 6a), monancestor and all descendants (node- whichwas Ž rstused in phylogenetic sys- based) orlimits inclusion to all descen- tematicsby Hennig (“stammgruppe”; 1969, dantscloser to one ormore of the reference 1983).Hennig’ s (1983:15)vague formulation taxa(stem-based) (de Queirozand Gauthier, ofthe conceptspeciŽ ed allextinct species 1992)(Fig. 1;Table 1).In node-based deŽni- “whichcan be shownprobably tobelong to tions,the phrase“ least-inclusiveclade” can aparticularmonophyletic group ofthe phy- replace “commonancestor and all descen- logenetic systembut whichare probably no dants”for cladists sensitive to the allusionto 340 SYSTEMATICBIOLOGY VOL. 48 ancestors(Lee, 1998).Listing included taxa (1993)and all of its descendants” ). Theseex- withouta relationalphrase about ancestry , amplesunderscore the need forclariŽ cation orsimply designatingtaxa as node- orstem- ofterms (T ables1, 2). basedwithout reference taxa,does not con- A node-stem triplet (NST)isa deŽnitional stituteaphylogenetic deŽnition, because the conŽguration involving three taxa,a node- boundariesof the taxonin questionare not basedtaxon composed of two stem-based speciŽed (de Queirozand Gauthier, 1990; subordinatetaxa (Sereno, 1997,1998; Fig. 8): Bryant,1996). TaxonA: Taxab andc, their mostrecent In the currentliterature, there existssome commonancestor, and all its descendants. confusionover what is necessary and sufŽ - TaxonB: All taxacloser to taxon b thanto cient fornode- andstem-based deŽ nitions. taxon c. Bryant(1996:185) suggested thata morein- TaxonC: All taxacloser to taxon c thanto clusive taxonbe insertedwithin a stem- taxon b. baseddeŽ nition, such as “ allmembers of taxonA thatare morecloselyrelated to taxon Bthanto taxon C.” Including taxonA, how- ever, isnot necessary and may lead to inter- nalconicts within the deŽnition (e.g., when taxonA isincluded withintaxon B orC on analternativephylogeny). Thegoalofa phy- logenetic deŽnition should be tounambigu- ouslyidentify aspeciŽc commonancestor given any arrangementof taxa, rather than toidentify suchan ancestoronly ona subset ofphylogenetic hypotheses. Meng et al.(1994) and Wyss and Meng (1996)introduced a “stem-modiŽed node- baseddeŽ nition” to effectively unite crown- group rodents,whose basal relationships areuncertain. Their preferred deŽnition of FIGURE 8.DeŽ nitional triumvirate termed anode- Rodentia(“ the cladestemming from the stem triplet, composed ofa node-basedtaxon (A) and mostrecent commonancestor of Mus and two subordinatestem-based taxa (B andC), which in- allRecent mammals more closely related corporates addedor repositioned taxa(dashed lines with daggers)without changingthe relative taxonomic to Mus thanto Lagomorpha or members content oftaxon A, B,orC (asexpressed bythe equiva- ofany other eutherian ‘order”’;Wyssand lence statementA=B+C).Adotindicates anode-based Meng, 1996:562)is better interpreted asa deŽnition; anarrow indicates astem-baseddeŽ nition. specialstem-based rather than node-based deŽnition, because ituses only one ingroup reference taxon( Mus)andone ormoreout- Taxab andc (notshown in Fig. 8)constitute group reference taxa(e.g., Lagomorpha). reference taxawithin taxon B andC, respec- Their deŽnition merely addsa phrase(“ the tively.Although notessential, the sameref- cladestemming from the mostrecent com- erence taxa(b, c) maybe used forthe trioof monancestor ”)toan otherwise typical taxain aNST, which then specify complemen- stem-baseddeŽ nition based on living ref- tary deŽnitions. The pairof stem-based sis- erence taxa.That phrase ensures inclusion tertaxa, in addition,may have reciprocal def- ofall extinct taxa within the crownclade. initionsthat utilize the samereference taxa Bryant’s (1996:185)reformulation of this in antipodalpositions. The word“ taxa”in deŽnition, on the otherhand, is clearly a the stem-baseddeŽ nitions listed above may node-based deŽnition, because he speci- optionallybe replaced byreference toa more Žed only ingroup reference taxa(“ the most inclusive taxon(Bryant, 1996). A stem-based recent commonancestor of the species re- deŽnition for Saurischia, for example, might ferred toRodentia by Wilsonand Reeder read,“ All dinosaursmore closely related 1999 SERENO—RATIONALE FOR PHYLOGENETICDEFINITIONS 341 toNeornithes than to Triceratops ” (Sereno, (Fig. 9,moves2, 3).For a taxonwith a basal 1998). dichotomy,analternative common ances- Taxonomicequivalence isa statement(or torcan be identiŽed only if one reference equation)in which one taxonis shown taxonis relocated to the opposing side or tobe equivalent in current and poten- outsidethe basaldichotomy .Are someref- tial taxonomiccontent to subordinate taxa erence taxamore likely tobe relocatedin this plus their commonancestor (T able 1). mannerthan others? The NSTdescribed aboveis composed ofa node-based taxon(A) andtwo subordinatestem-based taxa (B, C)and canbe writtenas the equivalence state- ment“ A=B+C,”because taxonA, by deŽnition, is equivalent totaxa B andC plus their mostrecent common ancestor.

PHYLOGENETIC DEFINITIONS: RATIONALE The Žrststep toward a phylogenetic tax- onomyinvolved the distinctionbetween deŽnition and diagnosis (Buck andHull, FIGURE 9.Three possible outcomes fromrelocation 1966;GrifŽ ths, 1973, 1974; Farris, 1976; Ghis- of areference taxon.1 =relocation onthe sameside of elin, 1984;Rowe, 1987). A secondstep in- abasaldichotomy hasno effect, 2=relocation to the volvedthe formulationof node- andstem- opposite side of the basaldichotomy identiŽes aless baseddeŽ nitions by use ofreference taxa inclusive commonancestor, 3 =relocation outside the andrelational statements about ancestry (de basaldichotomy identiŽes amore inclusive common Queirozand Gauthier, 1992). A thirdstep, ancestor.Reference taxaare encircled, andthe original basaldichotomy is shown with heavylines. outlined here, involvesthe speciŽcation of guidelines forselecting effective reference taxaand criteria for positioning node- and stem-baseddeŽ nitions. First,a taxonpositioned near the basal Phylogeneticrearrangements and introduc- dichotomyof a cladogramis always eas- tion ofnew taxa arethe principal factors ier torelocate to the opposing side (i.e., thatdestabilize taxonomic content. Stabil- requires fewer additionalsteps) than is a ityof taxonomic content is enhanced by nested taxon,if allother factors are regarded choosing(1) effective reference taxaand asequal amongingroup taxa(e.g., complete- (2) aneffective conŽguration of phyloge- ness,missing data, and homoplasy). Unlike netic deŽnitions. abasaltaxon (Fig. 5d),a nested taxonshares synapomorphiesthat increase its phyloge- Reference Taxa netic (patristic)distance from the common Position.—Given aparticularphyloge- ancestor(Fig. 5e).Thus, stability of taxo- netic hypothesis,the taxonomiccontent of a nomiccontent is enhanced in phylogenetic phylogenetic deŽnition is altered only if the deŽnitions if nested reference taxaare cho- reference taxaspecify analternative com- sen thatare located at some distance (at monancestor. Given abasaldichotomy with leastseveral nodes away) from the basal one reference taxonon each side, the iden- dichotomy.Thisdistance is easy to assess tiŽcation of the immediatecommon ances- quantitativelyfor various nested taxaon a toris not affected by relocationof a ref- given phylogeny. erence taxonon its side ofthe basaldi- Second, maximallyinclusive reference chotomy(Fig. 9,move 1). Relocation of taxa(Fig. 5c)have greater potential to cre- areference taxonto the opposingside or ateunnecessary taxonomic redundancy and toa locationoutside the basaldichotomy internalinconsistencies after relocation of identiŽes a different commonancestor taxa(Fig. 3).This is true forboth node- 342 SYSTEMATICBIOLOGY VOL. 48 andstem-based taxa. In the currentlitera- ture,maximally inclusive reference taxaare often used in phylogenetic deŽnitions. In their tetrapodclassiŽ cation, for example, de Queirozand Gauthier (1992:475) used suc- cessivemaximally inclusive reference taxa forall deŽ nitions— apattern here termed re- cursivereferencing (Fig. 10a).Recursive refer- encing canhave undesirable consequences because itshifts the burden ofa moreprecise deŽnition to a slightly lessinclusive higher taxon.This higher taxonmay not be de- Žned, orit too may be affected by analter- nativeconŽ guration of basal relationships. Salgadoet al.(1997), for example, chose Prosauropodaand Sauropoda as maximally inclusive reference taxafor Sauropodomor- pha.If abasalsauropodomorph is reposi- tioned,the deŽnitions of Prosauropoda and Sauropodamust be determined toassess po- tentialtaxonomic consequences. However , Salgadoet al. (1997) used Prosauropoda asa terminaltaxon without deŽ nition. Sauropodawas deŽ ned asa node-based taxonon the basisof two maximally in- clusive reference taxa, Vulcanodon and Eu- sauropoda(all othersauropods). Thus, if the incompletely knownbasal sauro- FIGURE 10.Referencing styles. (a)Recursive refer- pod Vulcanodon isreinterpreted asbe- encing selects asuccession ofthe most inclusive ref- ing moreclosely related to prosauropods, erence taxa.(b) Nested referencing selects thatsame Sauropodaand Sauropodomorpha would remote reference taxon.Reference taxaare encircled. become synonyms. If, onthe otherhand, Sauropodomorpha isdeŽ ned onthe basisof the nested ref- Taxawith numerous missing entries in a erence taxa—the prosauropod Plateosaurus phylogenetic analysisusually reduce phylo- andsauropod Saltasaurus (Sereno, 1998)— genetic resolutionby generating numerous achange in the phylogenetic position equally parsimonioustrees. W ell-known ref- ofany other prosauropod or sauropod erence taxa,even if they aresomewhat less hasno effect onthe taxonomiccon- nested,are preferable topoorly known taxa tentsof Sauropodomorpha or Sauropoda. (Fig. 11).A single poorlyknown basal taxon Sauropodomorphacan be deŽned as“ Pla- isleast stable and, therefore, leastdesirable teosaurus, Saltasaurus ,their mostrecent asareference taxon. commonancestor, and all descendants” ; Use withRecent orextinct Žlters .—“Recent” andSauropoda can be deŽned as“ all (“extant”or “ living”) or“ extinct”may be sauropodomorphsmore closely related to used in phylogenetic deŽnitions of crown Saltasaurus than to Plateosaurus .”Thephylo- andstem taxa, respectively ,tohelp tostabi- genetic positionof Vulcanodon hasno effect lize taxonomiccontent in the face ofpoorly onthe identiŽcation of respective common resolvedbasal relationships. For a crown ancestors. taxonwith a stem-baseddeŽ nition, a Recent Completeness .—Poorlyknown taxa are Žltercan restrict the boundariesof a clade morelikely tobe phylogenetically unsta- toliving taxa(Meng etal., 1994; Wyss and ble thanwell-known taxa(Wilkinson, 1995). Meng, 1996).Rodentia, for example, could 1999 SERENO—RATIONALE FOR PHYLOGENETICDEFINITIONS 343 be deŽned as“the leastinclusive cladecom- taxamore closely related to it than to any posedof Recent mammals more closely re- othercrown clade” (de Queirozand Gau- lated to Mus thanto Lepus.” For stem taxa, thier,1992:475). in contrast,a stem-baseddeŽ nition using an Listingmore than a pairof reference “extinct”Ž ltercan restrict inclusion to ex- taxadoes not seem tocompromise a node- tincttaxa when outgrouprelationships are basedphylogenetic deŽnition in anydis- uncertain.Moas, for example, couldbe de- cernible way.Node-based deŽnitions are Žned as“ allextinct species moreclosely constructedwith what may be termed in- related to Dinornis than to Struthio,” the ternal inclusion.A contradictoryrelation- ostrich. ship between multiple ingroup reference Number.—The number ofreference taxa taxafor a node-based deŽnition is im- thathave been used in phylogenetic deŽni- possible toconstruct with internal inclu- tionshas varied from two to inŽ nity .Gau- sion,because acladealways exists that thier (1986:14),for example, deŽned Avesas includes allingroup reference taxa.Multi- anode-based taxonincluding “alldescen- ple ingroup reference taxaeffectively stabi- lize the taxonomiccontent of a node-based taxonif basalrelationships are uncertain (Fig. 12a). Forstem-based deŽ nitions, multiple out- group reference taxaeffectively stabilizethe taxonomiccontent of a taxonif outgroupre- lationshipsare uncertain (Fig. 12b).Multi- ple ingroup reference taxafor stem-based deŽnitions can create a contradictorysit- uation,if one (ormore) ingroup reference taxaare repositioned closer to the outgroup reference taxon(Fig. 12c)or to a position outsidethe cladeas originally deŽ ned. In thiscase, the external inclusionfundamen- talto a stem-baseddeŽ nition creates a con- tradictoryrelationship among the original ingroup reference taxa,which areno longer moreclosely related to each other than to the outgroupreference taxon(Fig. 12c).In the example shownhere, relocationof ingroup FIGURE 11.Nestedness andcompleteness in the se- reference taxonD createsa contradictoryre- lection of reference taxa.A nested, well-known taxon lationshipwith a secondingroup reference is more likely to constitute astable reference taxon(en- taxonE, if taxonA hasthe stem-baseddef- circled). initionof “ alldescendants more closely re- latedto taxon D andE thanto taxon B.” An inclusive ingroup reference taxon,however, dantsof the mostrecent commonancestor canmanifest the sameproblems in thiscir- ofRatitae, Tinami, and Neognathae.” Three cumstance(Fig. 12c).If taxonA isdeŽ ned reference taxa,rather than two, were chosen, as“ alldescendants more closely related to presumably because ofunstated uncertainty taxonC thanto taxon B,” andif taxonC is in the phylogenetic relationshipsamong deŽned onthe basisof taxon D, acontra- these three aviansubgroups. De Queiroz dictorydeŽ nition results with relocation of andGauthier (1990:310, 1992:461) suggested taxonD asshown; taxon A nowsubsumes thatphylogenetic deŽnitions should utilize itsoriginal ingroup reference taxonC. Such only tworeference taxa—but then erected contradictorydeŽ nitions can be avoidedif deŽnitions for total taxa that used asrefer- anested ingroup reference taxon(or nested ence taxaone crownclade plus “allextinct taxa)are selected, such as taxon E, itsun- 344 SYSTEMATICBIOLOGY VOL. 48

FIGURE 12.The effects of multiple reference taxa.(a) Multiple ingroup reference taxaeffectively maintainthe taxonomic content of node-basedtaxon A when basalrelationships areunresolved orare unstable asa result of missing data.(b) Multiple outgroup reference taxaeffectively maintainthe taxonomic content ofstem-based taxon Awhen outgroup relationships areunresolved orare unstable asa result ofmissing data.(c) Inclusive ingroup reference taxonC ormultiple ingroup reference taxa(D andE) canresult in deŽnitional ambiguityfor stem-based taxonA when basaltaxon D changesits relationships; asingle, nested ingroup reference taxon,such astaxon E, is preferable in stem-baseddeŽ nitions. Reference taxaare encircled; adot indicates anode-baseddeŽ nition; an arrowindicates astem-baseddeŽ nition; adashedline indicates achangein position of abasaltaxon. labeled sistertaxon, or both. Most contra- resolvedpositions for relocation or addition dictorydeŽ nitions— which previously have oftaxa (Fig. 8).If taxaA, B,andC havestem- been citedas a general weaknessof stem- baseddeŽ nitions, the followingobtains with baseddeŽ nitions (Schander andThollesson, introductionof new taxaas shown. T axaB 1995)—are the resultof choosing maximally andC will incorporatean additional taxon inclusive reference taxarather than more- withno change in their relationshipwith nested relatives.Still, multiple ingroup ref- the basaldichotomy or with taxon A. When erence taxamay best be avoidedin stem- taxonA incorporatesa new taxon,however, baseddeŽ nitions. itis removed from the originalbasal di- chotomy;the taxonomiccontent of taxon A Node-Stem Triplet canno longer be expressed astaxon B plus Given taxonA andsubordinatetaxa B and taxonC, but rathermust include anaddi- C(asimple dichotomy),there areonly three tionaltaxon. If taxaA, B,andC havenode- 1999 SERENO—RATIONALE FOR PHYLOGENETICDEFINITIONS 345 baseddeŽ nitions, the followingobtains with ing dichotomiesin the historyof life are introductionof new taxa(Fig. 8).The taxo- labeled witha trioof taxon names suit- nomiccontent of taxon A isnot affected by able fora NST, suchas Dinosauria = Or- anadditionaloutgroup taxon, which is ex- nithischia+ Saurischia(Fig. 13).Naming all, cluded bydeŽnition. T axaB andC, however, oreven most,clades is not a heuristicen- areremoved from the basaldichotomy; the deavorthat would enhance communication. taxonomiccontent of taxon A, asaresult,is Second, NSTscannotbe constructedfor ad- nolonger taxaB andC andtheir mostre- jacentdichotomies on a cladogramwithout centancestor, but rathermust include two coining new companionnode- orstem- additionaltaxa. basedtaxa. An existingstem-based subor- Only one deŽnitional conŽ guration, a dinategroup ofone NST,suchas Ornithis- NST, preserves the taxonomiccontent of chia,cannot simultaneously function asa three taxaabout a dichotomy,asexpressed node-based group ofa less-inclusive NSTat by the equivalence statementA =B+C.A the baseof Ornithischia. A companionnode- NSTiscomposed of a node-based taxonand basedtaxon (composed of Pisanosaurus and twosubordinate stem-based taxa. Addition otherornithischians) would need tobe de- oftaxa to resolved locations around a NST Žned forthis less-inclusive NST(Fig. 13). cannotalter the simplestexpression of rela- Coining numerouscompanion taxa that dif- tivetaxonomic content, A =B+C. fer only in deŽnitional type but notin cur- When applying aNSTtodichotomies on renttaxonomic content will notenhance acladogram,two observations are note- communication.A complete NSTnetwork worthy.First,only asmallsubset of exist- wouldrequire node- andstem-based taxa at

FIGURE 13.Recognition ofNST sin the higher-level taxonomyof Dinosauria (fromSereno, 1998). Stem-based taxaare represented byan arrow (a) or regular typeface (b).Node-based taxa are represented bya dot (a)or boldface (b). 346 SYSTEMATICBIOLOGY VOL. 48 eachbranchpoint. A moreconservative ra- totalclades; (2) acladecomposed of two di- tionalefor placement ofNST satnamed di- verse subclades;(3) amorphologicallydis- chotomiesis considered below . tinctclade composed of two distinctive sub- clades;and (4) adichotomywith signiŽ cant TaxonomicFramework historicalusage. Placement of NSTs is based Taxonnames are applied toorganismal di- onfour criteriathat mirror these traditional versityas tags for identiŽ cation and infor- labeled dichotomies. mationstorage and retrieval (Farris, 1979). Survivorship .—Crown,stem, and total The followingkinds ofdichotomies have taxaare deŽ ned onthe basisof survivor- been “tagged”with a trioof names and ship (Table 1),which can provide the basis used mostoften by systematists:(1) ahigher- forNSTs (Fig. 14).The strengthof this crite- level crownclade with subordinate crown or rionlies in itsunambiguous interpretation.

FIGURE 14.Survivorship asthe basisfor supraspeciŽ c taxonomy.(a)Indented crown-total taxonomyempha- sizingthe association between atotal taxonand its less inclusive crown taxon(de Queiroz andGauthier, 1992). (b)Indented crown-total taxonomyemphasizing NST structure. (c) Indentedcrown taxonomyomitting total taxa. (d)NST (shaded)form the frameworkof a crown-total taxonomy.Regulartypeface (a–c) oran arrow (d) indicates astem-basedtaxon; boldface (a–c) ora dot (d)indicates anode-basedtaxon; daggers indicate extinct taxa. 1999 SERENO—RATIONALE FOR PHYLOGENETICDEFINITIONS 347

Itis highly unlikely thata species believed to Adiversity-basedNST recognizingDi- be extinctwill be discoveredalive and vice nosauriaand its two diverse subclades,Or- versa.The rapidextinction of the modern nithischiaand Saurischia, ties these three biotais a notableexception (Lucas,1992); se- taxato a majordichotomy in the evolu- lectionof a particularhistorical datum (such tionof archosaurs (Fig. 13a).T raditionalsys- asthe beginning ofthe Recent) mayat least tematistshave maintained this dichotomy partiallyside-step thisproblem. NSTsbased by interpreting newly discoveredbasal di- onhigher-level crowntaxa and their asso- nosaursas either basalornithischians or ciatedsubordinate total taxa form the back- basalsaurischians and by excluding out- bone ofthe tetrapodclassiŽ cation proposed groupsfrom Dinosauria. The only wayto by deQueirozand Gauthier (1992). Because dissociatediversity and a diversity-based these authorsemphasized the relationship NSTpositionedat Dinosauriais to relocate between acrownclade and its more inclu- the deeply nested reference taxa Triceratops sivetotal clade (as shown by their indented andNeornithes outside of Ornithischia and classiŽcation; see Fig. 14a),the NSTstruc- Saurischia,respectively (Sereno, 1998). ture oftheir classiŽcation was not discussed Morphology.—Some taxaare more distinc- andis not immediately apparent. Their clas- tivemorphologically than others. Phyloge- siŽcatory scheme, nevertheless, consistsof netic analysisof morphological data rarely subordinateNST sthatcan be tabulatedas distributesapomorphies evenly across anindented crown-totaltaxonomy (Fig. 14b, nodes,and those nodes characterized by d). One canlist only crowngroups (a crown profound transformationsare often the sub- classiŽcation; Fig. 14c),although the pur- ject ofbiological discourse. A morphology- poseof such a classiŽcation is not immedi- basedNST recognizesa dichotomybounded atelyapparent, given the inclusionof many by numerousapomorphies (Fig. 15b).The extinctspecies withincrown taxa. number ofapomorphies (or the sizeof the Diversity.—Relativediversity is an impor- morphologic“ gap”), however,is less sta- tantconsideration in the erectionand posi- ble thandiversity as a criterionfor distin- tioningof higher taxonnames. Some groups guishing somebranchpoints from others. aremuch morediverse thanothers, and this Discoveryof new taxainevitably entails difference isoften accordedbiological sig- the splittingof morphologic “ gaps,”and niŽcance. On acladogram,the simplestdi- alternativeoptimization of character data versitycomparisons are between sistertaxa withmany missing entries mayalso dra- oneither side ofa dichotomy(Fig. 15a).A maticallyshift the locusof character-state diversity-basedNST stabilizesthe associa- change. tionof taxon names around a dichotomythat Some morphologic“ gaps,”nonetheless, involvesdiverse sistergroups and several haveremained remarkablystable, partic- low-diversityoutgroups. A diversity-based ularlythose among extant species asso- NSTtiestaxa to diversity ,despite relocation ciatedwith a poor,or nonexistent, fos- oraddition of taxa near the basaldichotomy . silrecord. Gap-bounded dichotomiesalso There isonly one wayin whicha diversity- occuramong extinct taxa. The distinctive basedNST canbe alteredto dissociate the cladeSauropodomorpha, for example, is namedtrio of taxa and high diversity:relo- composedof the distinctivesubclades cationof most of the diversityof one ofthe Prosauropodaand Sauropoda. Despite sistergroups but notthe included reference morethan a century ofdiscovery ,morpho- taxon.Alternatively ,one couldview this logicallyintermediate species haveyet to dissociationas the relocationof a reference be uncovered thatsigniŽ cantly reduce the taxonbut notof the majorityof its previously distancesat thisdichotomy .Amorphology- associateddiversity .Such phylogenetic rear- basedNST atthis dichotomy re ects his- rangementsare unlikely (with nested refer- toricalexperience— that newly discovered ence taxa),and diversity remains one ofthe sauropodomorphshave been positioned leastambiguous and most stable criteria for amongknown prosauropod or sauropod establishingNST s. taxa,whether thisis the resultof punctu- 348 SYSTEMATICBIOLOGY VOL. 48

FIGURE 15.Criteria forpositioning NST.(a)Diversity-based NST,in which two high-diversity taxahave succes- sive low-diversity outgroups.(b) Morphology-based NST, in which adistinctive (particularly apomorphic) taxon is composed oftwo distinctive subordinatetaxa. (c) Tradition-basedNST, in which ataxonand its subordinate taxahave a longhistorical association. atedevolution, temporal gaps in the fossil a“feather”or“ wing”will be scoredand record,or chance. interpreted in different waysby different Tradition.—Some taxonomicnames have systematists.Likewise, the long-standing along-standingassociation with a particu- associationof several of these “key”synapo- lardichotomy .Mostoften thisassociation is morphieswith Archaeopteryx andOrnithu- basedon a “key”character or set of charac- raeclearly is oversimpliŽ ed (Chen et al., tersand involves a taxonthat is transitional 1998;Ji et al.,1998). Still, the nameA vesmay in form(i.e., a“missinglink” bounded by be better applied toits traditional dichotomy morphologic“ gaps”). Forthe pastcentury , (Fig. 15c;Lee, 1996;Sereno, 1998)than re- forexample, “Aves”has been associated locatedto a distantnode, such as crown- withthe dichotomybetween Archaeopteryx group avians(Gauthier, 1986), even if only to andOrnithurae,a taxoncomprising all other avoidconfusion on the partof the majority birds(Fig. 15c). Archaeopteryx preserves ofbiologists. A tradition-basedNST placed evidence offeathers, wings, a perching foot, atthe dichotomybetween Archaeopteryx and andother striking adaptations reminiscent Ornithuraestabilizes the long-standinghis- ofthose of living birds.Surely ,however, toricalinterpretation of A vesand maintains 1999 SERENO—RATIONALE FOR PHYLOGENETICDEFINITIONS 349 aclose,albeit imprecise, association between Avesand synapomorphies involving mod- ern feather,wing, andpedal design. The four criteriadiscussed above are nei- therexact nor mutually exclusive. The num- ber oftaxa or apomorphies characterizing “high diversity”or “ morphologicallydis- tinct”clades, respectively ,isrelative and im- precise. Of the four criteria,morphology- baseddichotomies are least useful, because they arerare and relatively unstable over timeand can exist solely as artifactsof miss- ing data. Thebestcase for location of a NSTismade when severalof the criteriadescribed above pointto the samedichotomy ,asis the case withthe nodeDinosauria.Within dinosaurs, the ceratopsidsubgroups Ceratopsinaeand Centrosaurinaeprovide anotherexample, eachmore diverse anddistinctive than their nearestoutgroups (Fig. 16).When criteriafor placement ofa NSTdisagree,or when the FIGURE 16.NST amongceratopsian dinosaurs basedon the criteria outlined in Figure15. Num- proximityof another NST wouldnecessitate berof generafor each terminal taxonare shown coining new companiontaxa, a NSTneed within circles, which highlights the diversity ofcer- notbe established(e.g., the dichotomyin- atopsid subclades ascomparedwith the outgroups. volvingSaurischia, Sauropodomorpha, and Thethickened clade lines arescaled accordingto Theropoda;Fig. 13a). the numberof synapomorphiesthat diagnose each Subdivision ofone group intotwo clade, which underscores the morphologic dispar- ity of Ceratopsidaeand its two subgroupscom- subordinategroups is the simplestform of paredwith adjacent,more inclusive nodes(scale nonredundantordination in taxonomyand barequals 20 apomorphies;Sereno, 1998). The in- reects the mostprevalent phylogenetic pat- dented classiŽcation reveals acentury-long tradi- tern.The principal reasonsthat these di- tion thatrecognizes Ceratopsidaeand its two sub- chotomieswere namedin the Žrstplace was groups.Node-based taxa are represented bya dot toacknowledge survivorshipto the Recent, (orboldface), and stem-based taxa are represented toreference large-scalepatterns in diversity, byanarrow (or regular typeface). andto record major changes in morphology. Maintainingthe integrity ofsuch named di- chotomiesis a heuristicendeavor in con- node-based andstem-based deŽ nitions, certwith the aimsofphylogenetic taxonomy manifestmany of the sameambiguities andcan be achieved by judicious choiceof thathave long been associatedwith tra- nested reference taxaand the NSTconŽgu- ditionalcharacter-based taxa. rationof phylogenetic deŽnitions. 3.Crown taxa are deŽ ned withliving ref- erence taxa,but they require animme- CONCLUSIONS diateoutgroup that is extinct. Crown The foregoing critique oftaxonomic def- taxaare not demonstrably more stable initionshas resulted in the followingmajor orinformative than stem or total taxa, conclusions: and“ widely used”higher taxonnames havenotbeen historicallyassociated with 1.Currently there isno clear rationale for crown taxa. formulationand placement ofphyloge- 4.Stem taxaare restricted to extinct clades netic deŽnitions. (orspecies) whoseimmediate outgroup 2.Apomorphy-based deŽnitions, unlike includes atleast one living species.De- 350 SYSTEMATICBIOLOGY VOL. 48

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