The Role of Parsimony

8/3/2019 The Role of Parsimony.

1/20

Z. 2001. Syst . Evolut . - forsch. 31 (1993) 1-200 993 Verlag Paul Parey, Hamburg und BerlinISSN 0044-3808

Received on 30. October 1991

Zoologiscbes Institut der C hristian-Albrechts- Universitat Kiel, FRGThe role of parsimony, outgrou p analysis,and theory of evolution in phylogenetic systematics

By S . L O R E N Z E N

A b s t r a c tI t is ar ued that both the principle of parsim ony and the theory of evo lution , especially that ofnatur afsele ction , are essential analytical tools in phylogenetic systematics, whereas the widelyused ou tgro up analysis is com plete ly useless and m ay even be m isleading.In any systematic analysis, tw o types of attern s of characters and character states must bediscriminated which are referred to as compf%ely and incom pletel y resolved. In the forme r, a l lknown species are presented in which the characters and their states studied occur, whereas inthe latter this is no t the case.Dep endent on i ts s t ructu re , a pat tern of characters and their s ta tes may be explained by e i thera uni ue or by various conflic ting, equally most pars imon ious h potheses of relationships. Theso-ca?led permutation method is introduced which facili tates Jnding the conflicting, equallymos t pa r s imonious hypo theses of r e la t ion sh iy . The ,u t i li ty of the principle of pars imony isl imited by the uncer ta inty as to whether i ts app ication in systemat ics mu st refer to the m inim umnumber of steps needed to ex lain a pa t te rn of character ts and their s ta tes m ost pars imonious1or to the minim um num ber ofevolu t ionary events assumed to have caused these s teps . Al thougthese num bers may differ, the form er is usually preferred for simplicit EIo n test samples and jad is t ic type of outgrou p analysis. Essent ia l ly , the orm er is used Y r analys-The types of out roup analysis are show n to exis t which are te rm el fa rs im on y anal s is baseding incompletely resolved patterns of characters and their states, the latter for analysing com -plete ly resolved ones . Both typ es are sh ow n to be com plete ly useless for rejecting even on e ofvarious conflicting, equally mo st parsim onio us hypothe ses of relationshi sAccord ing to con tem ora ry knowledge , th i s ta sk can be acco m pl i sh e~ on ly y employ ing thetheory of evolu t ion ( incLding the the ory of natural se lect ion) . But even then, m any ph lo enetic-systematic problems will remain unsolved. In such cases, arbitrary algorithms li le $0,:offered by phenetics can a t best offer pseudosolu t ions to open problem s.Despi te i ts l imita t ions , phylogen et ic sys temat ics is super ior to any kind of aphylogenetic sys-temat ics ( t ransform ed cladis t ics included) in approac hing a (no t : the) general reference sys tem of organisms.Key words: Phylo enetic systematics - Transform ed cladis t ics - Pars imo ny analysis - T h e o r yof evofution - Ou tgro up ana lys is

The problem: Must phy logenetic systematics rely on the theory of evolution?T a x o n o m i s t s of a l l t a x o n o mi c s c h o o l s a g r e e t h a t b i r d s , ma mma l s , i n s e c t s , s p i d e r s , g a s -t r o p o d s , c e p h a l o p o d s , n e m a t o d e s , e t c . a r e we ll c h a r a c te r i z e d v a li d ta x a . T h i s is r e m a r k a -b l e, s i nc e s o m e t a x o n o m i c s c h o o l s a r e b a s e d o n t h e t h e o r y of e v o l u t i o n (= t h e o r y ofn a t u r a l s e le c ti o n p l u s t h e o r y of d e s ce n t) , w h e r e a s o t h e r s a r e n o t . W h e n the u s e of thet h e o r y of e v o l u t i o n is a p p a r e n t ly u n i m p o r t a n t f o r r e c o g n i z in g t h e m e n t i o n e d t ax a , w h ys h o u l d w e n o t g e n er a ll y try to p e r f o r m a p h y l og e n e t ic s y st e m a t ic s w i t h o u t r e f er r in g t o t h et h e o r y of e v o l u t i o n ? E v o l u t i o n a ry biologists mi g h t i n t e r p r e t t h e r e s u lt s t h u s a c h ie v e d i nt h e l ig h t of t h e t h e o r y of e v o l u t i o n , c r e a t i o n i s t s in t h e l i g h t of c r e a ti o n is m , a n d t h o s e n o ti n t e re s t e d i n a n y i n t e r p r e t a t i o n a t a ll c o u l d a c c e p t t h e re s u l ts a s t h e y a r e. We c o u l d h o p e tof ina lly c rea te the genera l r e fe rence sys tem(HENN 1G 1966:7).U. . Copy r igh t C lea rance Cen te r C ode S ta tement : 0044-3808/93/3101-0001/$02.50/0


2/20

2 S.LorenzenAccording to H E N N I G ,his would be a phylogenetic system, i. e. a system show n to beentirely composed of holophyletic taxa (= mono phylet ic taxa sensu HEN NIG )inked to-gether by a dichotomou s tree of genealogical relationship s.Phylogenetic systematics sensu H E N N I Cnd his suppo rters is based o n the theo ry ofdescent . The e xtent to which i t is based o n the the ory of natural selection as well has notbeen fully explored u p to now, but it is widely agreed that an adeq uate app lication of thelatter theor y wo uld at least sup po rt any phylogenetic-systematic analysis .Phenetics (= numerical taxonomy) was never based o n the theo ry of evolution, i . e. itwas always a kin d of aphylog enetic systematics: Not only do we insist on the separation

of phenetic from phylogenetic considerations in taxonomic p roced ure, b ut we also feelthat on ly phenetic evidence can be used to establish a satisfactory classification. (SNEATHand SO KAL 973: 10).Since the en d of the seventies, the claim has been advanced th at even phylogenetic sys-tematics can and mus t be performed witho ut referring to any par t of the theory of evolu-tion. Thi s means that a phylogenetic system could and sh ould be achieved by employing akind of aphylogenetic, pre-evolutionary systematics. This mo dern typ e of phylogeneticsystematics is called transform ed cladistics, m od er n cladistics, or simply cladistics by itspr op on en ts (e. g. PLATNICK 980; PATTERSON 1980; E LD R ED C E nd CRACRAFT980;BRAD Y 1985), and neocladistics, pattern cladistics, natural or de r sy stematics, orm ain stre am cladistics by its critics (e. g. CARTMILL981; BEA TIY 982; CHARIG982;SZALAY nd BOCK 1991). As phylog enetic systematics sensu HENNIGas been termedcladistics by MA YR 1969: 70) and many subsequent authors , i ts t ransform ed vers ionwill be re ferred to as transforme d cladistics th ro ug ho ut this paper. Th e chief sym pto m ofthis change (i. e. f ro m p hylogen etic systematics sensu HENNIGo transfo rme d cladist ics)is the significance attached to the no des in cladogram s. In HEN NIGS oo k, as in all earlierwork in cladistics, the nodes are taken to represent ancestral species. Th is assumption hasbeen fou nd to be unnecessary, even misleading, and may be drop pe d. (PAITERSON980:239).Transform ed cladistics is based o n three general assumptions w hic h serve as guide-linesof the journ al Cladist ics.1. Features shared by organism s (homologies) manifest a hierarchical patte rn in nature.2. This hierarchical pattern is most economically expressed in branching diagrams, or

3. T h e nodes in cladograms symbolize the homologies shared by the organisms group edTransformed cladistics try to apply only two analytical tools for inferring cladogramsfrom o bserved patterns of characters and character states. Th ese tools are- the principle of parsimony and- the outgr oup comparison m ethod.M od er n phy loge netic systema tics as advanc ed by W ILEY 1981), A x (1984, 1987, 1988),RIDELY 1986), SLU YS1988), and others c on for ms wit h transformed cladistics in relyingprimarily o n these tools an d in claiming that phylogenetic systematics is indep ende nt ofthe theory of natural selection. A con trary view has been advanced by BO CK nd WAIILERT(1965), BOC K (1981), PE TERS nd GU TM AN N1971), PET ERS 1976), SCH MIT I. 1985),SZALAYnd B OCK 1991), and o thers.T he principle of parsimon y is generally accepted in science, phylog enetic systematicsincluded. It requires minimizing the number of assumptions when t rying to explainan unknown, but apparently exist ing coherence between observed phenomena. If theassumptions are clearly defined and accepted, results of the respective parsimony ana-lysis are indeed co mp ulsory in b oth phylogenetic and aphylogenetic systematics. Ho w-ever, a patte rn of characters and character states may ha ppen to be explainab le by variousconflicting, equally most parsimonious hypotheses of relationships. In these cases, a

cladograms.by the node , so that the cladogram is syn on ym ou s with a classification.


3/20

Parsimvny, ou tgroup analysis, and theory vf evolution in phylog enetic systematics 3further analytical tool is needed fo r rejecting som e of them and accepting the remaining aswor thy of furthe r analysis.If the o utg rou p comparison meth od is accepted as the only furthe r analytical tool avail-able in systematics, its application must be helpful in mastering the task outlined. Ot he r-wise i t would be completely useless. If even the th eor y of evolution is accepted as a furth eranalytical tool in systematics, its application, too, must be helpful in mastering the taskoutlined. Otherwise, phylogenetic systematics would be aphylogenetic.So, if phylogenetic systematics is to be evaluated, an answer m us t be provided to theques t ion whether the outgroup comparison method and the theory of evolution (thetheory of natural selection included) can provide any help in selecting amo ng conflictingequally most parsimonious hypotheses of relationships inferred from any observedpattern of characters and character states. The pre sent pap er is aimed at finding an answer

to this question.How to start a phylogenetic-systematic analysis

In both phylogenetic systematics and transformed cladist ics it is of crucial importance toestablish hypotheses on the holophyly of species sets. Each of these sets contains thewhole of all kno wn species in which o ne or several hom olog ous characters are show n tobe either present o r secondarily absent. Therefore, a ny phylogenetic-systematic o r trans-formed cladistic analysis must begin by examining the exact extent to which charactersand character s tates s tudied occur a mo ng all kno wn species. It is very im porta nt to clearlystate wheth er this task has been accomplished satisfactorily. R ath er ofte n in the literat ure,the method of phylog enetic systematics and transformed cladistics are introduced wit ho utemphasizing the importance of this poin t .Both characters and character states are diagnostic features tha t allow struc tur es andorganisms to be recog nized, distinguished f rom oth ers , and classified. These classifica-tions need n ot be phylogenetically relevant as is demonstrated by each determination keyor by classifying species according to their life styles into plankton, benthos, meiofaunaetc. In th e following, the terms character an d character state will always refer to th e pre-sence (and n ot to the absence) o r certain stru ctu res and peculiarities.Regardless of any m odifications, a ny presence of a struc ture will be termed a characterlabelled with 1, 2, 3, etc. th rou gh ou t this paper, whereas any modification of a s t ructurewill be termed characterstate and labelled w ith 1a, 1b, . . , 2a , 2 b, . . . etc.Whenever organisms of different species are fou nd t o c orresp ond in a certain charactero r character state, at least the first two of the three so-called m ain criteria of homology( RE M A N E956) mu st be applied to determin e wh eth er these species really display th e samecharacter or character state in the sense of OWENSriginal, aphylogenetic meaning ofhomology: Homologue- he same organ in different animals under every variety ofform and func t ion . (OW EN 843, citation fro m NAEF926: 410). Th e three main cr i teriaof homo logy are the fol lowing: 1. Cri ter ion of same relative po sitio n of a structu re withinthe context of other structures; 2. criterion of same special q ual ity of s t ructures ; 3 . cri-terion of linking different extreme modifications of a basic stru ctu re by transitiona l forms.Essentially, t he third criter ion is an auxiliary on e, as it allows exam ining, wh ether th e firsttwo criteria may be rega rded as being fulfilled even in difficult cases.It is importa nt to note tha t the application of the three main criteria cann ot reveal anymore than the sameness of a character or character state present in different species,regardless of theories explaining the causes of such sameness. Th at is , s tatements o n thesameness of characters an d character s tates do n ot involve any notio n on the single o rmultiple origin of the latter. Therefore , the fulfillment of the three ma in cri teria of ho mo-logy is only necessary but not sufficient for substantiating any phylogenetic statementon homology. The sameness of a character o r character s tate presen t in different or-


4/20

4 S. Lorenzenganisms will be designated a potential homology o r a potentially hom olog ous character o rcharacter state or simply as a character or character state of the respective organisms.Whether these characters and character s tates may be regarded as homologous in aphylogenetic sen se as well, requires an additional analysis based o n b ot h the principle ofparsimony a nd the theory of evolution. This will be necessary onl y in a mo re advancedstage of a phylogenetic-systematic analysis.The analysis outlined is completed as soon as each potentially homologous characterand character s tate s tudied is affiliated to i ts co rresponding maximum set of knownspecies. Such patterns will be referred to as completely resolved patterns of characters an dcharacter states. Otherwise, they will be referred to as being incompletely resolved. Pat-terns of the lat ter sort are often provided by studies on molecular characters . In bo th co m-pletely and incompletely resolved patterns of characters and character states, t he speciessets will be op en to further, yet un kn ow n species characterized by the corre spon ding char-acters o r char acter states, respectively.

Species sets each characterized by on e o r several potential homo logies m ay be encaptico r non-encaptic to each other, i . e. these sets may b e non-overlapp ing o r overlapping, re-spectively. In t he en captic case, a certa in set of species includes a differently characterized,smaller or equally voluminous on e completely o r no t at all , o r is included completely ornot at all in a larger set of species. Each case of comp lete inclusion will be referred to asinclusive encapsis, each case of comp lete exclusion as exclusive encapsis. In the non-encapticcase, a certain set of species includes anothe r set of species only partially. Quite early,HEN N IGe.g. 1949: 136) used the term encaptic in the outl ined sense. In transformedcladistic literature, the term encaptic is often replaced by compatible o r congruent, andthe term non-encaptic by incompatible o r incongruent. Since these terms are not quitecorrect in that context, encaptic and non-enca ptic are preferred.In accordance with the theory of evolution, a potentially homologous character orcharacter state may be absent in certain species du e to two reasons:- Eith er it was never present in any ancestor of these species,- o r it was present som ewh ere in th e ancestry of these species and wa s subsequently lost.These two forms of absence will be term ed primary and secondary absence of a charactero r character state, respectively. Ra the r often in literature, secondary absence of a charac-ter is equivocally termed secondary loss of that character, al though simply loss ismeant.P roponent s of the theory of evolution agree that gill slits are primarily absen t in Pro to-stomia and secondarily absent in adult Tetrapoda, o r that wings are primarily absent inCollembola and secondarily absent in Siphonaptera. Apparently, there are certain pos-sibilities of substantiat ing hypotheses on primary o r secondary absence of homologouscharacters an d character states in indicated species sets.

Co nd itions allowing the inference of on ly one or rather various m ostparsimonious hypo thesis of relationships from a pattern of characters andcharacter statesAs long as the theory of evolution is no t employed in systematics, any app lication of th eprinciple of parsimony means minimizing the number of assumed steps (origins, losses,or m odifications of characters) when trying to infer most parsimonious hypotheses of re-lationships from observed pa tterns of characters and character states. It sh ou ld be stressedthat an y modification of a character means that a pri or state was replaced by a subsequentone, i. e. that a single step involves bot h th e loss of a prior and th e origin of a subsequentstate (for examples see Figs. 3 and 6 ) . It was necessary to int roduce a new graphical symbo lto repr esen t such features adequately.


5/20

Parsimony, outgr oup analysis, and theory of evolution in phylogen etic systematics 5

12345

a

A B C D1 ~ 1 1 1 1 1 1 1 ~ 1 1 1 1 1 1 ) .

2 0 13 0 1C

I b n .l c 0d

: c h a r a c t e r p r e s e n t , - : charac ter absent0. a s s u m e d o r i g in ( or loss (X of a character[x..:I,}[ c h a r a c t e r a s s u m e d t o h a v e o r i g in a t e d in t h e i m m e d i a t e c o m m o n.IIIIIIII(XI a n c e s t o r of t he respec t i ve se ts of s p e c i e sFig. I . These enca tic ( i. e. non-overla ping) patterns of characters (a-c) and character states (d)are each exp lain ejm ost parsimoniousry by a single hypothesis of genealo ical relationship s; theo n l y s te s assumed refer to unique origins of the res ective characters an3 character states. Thesmall tagles to the right of the roots display the num ler of origins (+) and losses (-) per charac-ter. Basal and intermediate nodes refer to h pothetical ancestors; for s ace saving reasons, o n l ysteps assumed to have occurred are depictecrin these nodes. N ote that tge diagrams may be bi- ormultifurcating, and that ( i f the pattern s are completely resolved) nor. al l species sets grou ed bynodes m u s t be holo hyletic (for example: B in Fig. 1 c is not holophyletic). The symboi usedrefer to all figures o8 h is paper

To an evolutionary biologist , the num ber of steps assumed m us t not necessari ly corres-p o n d to t h e n u m b e r of evolutionary events w hich are assumed to have caused th ese steps.Theoretically, o ne evolutio nary event could be the cause of several steps .If only s teps a re counted in t ry ing to explain a certain patte rn of characters and theirstates most parsimoniously, the theoretical minim um num ber of steps to be a ssumed mus tbe at least equ al to t h e n u m b e r of characters o r - f considered -of character states stud ied.Any equali ty of both num bers i s only possib le if the patterns of characters are encaptic .Within these pa t te rns , only those a re found to be explainable by a single mos t parsim oni-o u s hypothesis of relationships w hich

- consist of characters, wh ereb y their states are neglected (for exam ples see Fig. 1 a-c), or- additionally deal with character states arranged by inclusive encapsis (for an exampleIn these cases, th e on ly steps to be assumed m ust refer to unique origins of these charactersand character states, as any assu mp tion of a loss would require the addi t iona l assumpt ionof a prior origin , i. e. of tw o steps altogether. Because of the i r uniqu e or ig ins , pro pon entsof the theo ry of evolution m us t regard these characters and character states as homologies(in a phylogenetic sense) of th e corre spo ndi ng species sets. Dep end ing o n the individualstructures of these patterns of hom ologies, th e result ing diagrams of relationships may bestrict ly dicho tom ous (l ike diagrams a, b and d in Fig. 1) or may inc lude polytom ies ( likediagram c in Fig. 1).

(XI : c h a r a c t e r a s s u m e d t o be pr imar i l y (0)r secondar i l y (m) bsent. assumed sub st i tu t ion of a pr ior by a subsequ ent character s ta te

whichFig. 1 d).


6/20

6 S. LorenzenTh e only o th er patterns each explainable by a single mo st parsimonious hypothesis ofrelationships are fo un d referring- to certain non-encaptic patterns of characters, whereby different states of these charac-

ters, if regarded at all, must be arranged by inclusive encapsis (for examples see Fig. 2).In these cases, t he n um ber of steps assumed is always higher than the nu m be r of charactersstudied. Th at is, these hypoth eses require th e assumption of at least tw o steps in the caseof at least o ne potentially h om olog ous character. These steps may refer to independentorigins (as in character 2 of Fig. 2 a an d ch aracters 2 and 4 of Fig. 2 b) o r to at least oneorigin and at least one sub sequ ent loss of a character (as in character 1 of Fig. 2 c). In thecase of in depe nde nt origins, a character can n o longer be regarded as a potential ho molo gyof its species set originally regarded, but rath er of different subsets of this set as indicatedby the respective hypothesis of relationships. In the case of on e origin an d at least on eloss, however, a chara cter continues to be a potential ho mo log y of its species set originallyregarded.

From a theoretical p oint of view, it is interesting to no te that the pattern of Figure 2 amay be co nt inued by adding fur ther potentia lly homo logous characters (4, 5, 6 , . .) andfurther maximum species sets (DE, EF, GH, ...) affiliated to them, respectively (seeFig. 2 b). When ever su ch a pattern deals with an uneven num be r of characters, it may beexplained by a single most parsimonious hypothesis of relationships dealing exclusivelywith presence a nd prim ary absence of characters. I n the case of thr ee characters (Fig. 2a ),this hypothesis would require assumption of four steps, in the case of five characters(Fig. 2 b) of seven and, generally, in the case of (2 n + 1) characters, of (3n + 1 ) steps. Th edifference between steps and characters is ( 3 n + 1) - (2 n + 1) = n, whereby n may bearbitrarily high bu t m us t at least be equal to 1.Apparently, even the pattern of Figure 2c may be con tinued by adding further triplesets of species each equivalently characterized su ch as the t w o of Figure 2c. In all of thesecases, the single most pa rsimoniou s hy pothesis deals with presence, and p rima ry and sec-ond ary absence of characters . T he hypothesis of Figure 2 c deals with five characters and

a

111111 11111115% *'2 0 - I )c 3 0 I/4 0 I5 0 I I

Fig. 2. Even these non-encapt ic character pat tern s are each explained mo st parsimoniously by asingle hypothesis of genealogical relat ionshi+s. Secq ndar y absence of characters m ay not (a-b)or may (c) be included in these hypotheses. he cladist ic ty pe of ou tgro up ana lysi s cannot y i e ldunequivocal resu l ts o n pr im ary and seconda ry absence of characters involved in these pat te rns


7/20

Parsimony, outgroup analysis, and theory of evolution in phyloge netic systematics 7

Fig. 3 . If characters and their s ta tes a re arranged enca tically such pa tter ns may be explained byvarious e ually most parsimonious hypotheses of refationshps; ei ht of more than twenty areillustrate] here. According to hypotheses a-e, either character 1 or ckaracter 2 or both charactersare assumed to have multiple originsseven steps. Generally, the continued cases deal with (2 n + 1 ) characters and (3n + 1 )steps, tha t i s , the d if ference be tween these tw o n um bers am oun ts to (3 n + 1) - (2n + 1 ) =n, w hereby n may be arbitrari ly high bu t mu st at least be equal to 2 .From the examples just ana lysed, the fo l lowing imp ortant conclusion may b e draw n:The d i fference be tween the m in imum num ber of steps to be assumed and the num ber ofcharac ters deal t wi th c anno t revea l anyth ing abou t the possib le nu mb er of rival hypothesesof relationships explaining a given pat ter n of characters most parsimoniously.All patterns other than the outl ined are always explainable by var ious, equal ly mos tparsimonious hypotheses of relationships. T hes e patterns include- all encaptic patter ns of characters and th eir states, as far as th e lat ter are arranged b y- most of non-encaptic patterns of characters, regardless of wh eth er their states are neg-In the former, encaptic case, various most parsimonious hypotheses of relationships arepossib le , s ince the charac ter s ta tes may be a rranged di f fe rent ly in branched o r unb ranch ed

exclusive encapsis (for an exam ple see Fig. 3), as well aslected o r considered (fo r examples see Figs. 4 and 5).


8/20

8 S.LorenzenA B Cwinged winged Siphon-Hemimetabola Holometabola aptera

a-I wings .holometaboly - rn

Fig. 4. The most simple non-encaptic ( i . e. overlapping) character pattern displayed a t the topmay be ex lained most parsimo nious ly b f o u r conflicting hypotheses of genealogical relation-ships (a). +he number is reduced to two, i r 3 happens to be a furth er character exclusively presentin a l l species of BC (b) . No te t h a t all hypotheses of grou I (secondary absence of characters doesnot oc cu r) differ from those of group I1 (secondary agsence of characters does occur) not bytheir branching orde rs, but rather by their statements on the homology of the characters studied

sequences: Th e pa t te r n of Figure 3 is explainable by over twen ty equal ly most pars imoni-ous hypotheses of relationships.W ithin the non-encapt ic case, th e mo st s imple of these pa t te rns i s depic ted a t the top ofFigure 4: Th e potent ial ly ho mo logou s charac ters 1 and 2 are affiliated to the species setsAB an d BC, respectively. If no fur the r charac ters a re regarded, any most pars imoniousexplanation of th is pa t te rn requires the assum pt ion of three s teps. Fo ur equal ly most par-s imonious hypotheses of relationships are possible in this case. Two of them deal exclu-sively wi th pr im ary absence and presence of the respect ive chara ters , w hi le the o t her t wodeal wi th s econ dary absence of charac ters as wel l. T he form er two hypotheses a re group edtogether to g r o u p I, the la t te r to g r o u p 11.In t ry ing to reject any of these mo st pars imonious hypotheses , on e could seek fur thercharacters ap pro pri atel y affil iated to the species sets regarded. If , f or example, th e pot en-t ia lly hom ologo us charac ter 3 is affiliated t o th e species set BC (as in Fig. 4b) , the inc lu-sion of th is charac ter in the hypotheses I a and I I a would require the assumpt ion of tw osteps, respectively, in the hypotheses I b an d I I b , however, of on ly one . Th e re fo re , the


9/20

Parsimony, outgroup analysis, and t heo ry of evolution in phylog enetic systematics 9hypotheses Ia and I Ia m ust be rejected, w hereas hypotheses I b and I1 b must be acceptedas wo rth y of furth er analysis. If, however, cha racter 3 is affiliated to th e species set CD (asin Fig. 2a), hypotheses Ib , H a, and I I b mu st be rejected, whereas hypothesis I a is ac-cepted. In systematic practice, however, character patterns are no rm ally not sup ple me nte dby fur the r characters in that favourable way.The hypotheses of Figure 4 display a striking feature: Th os e of gr oup I differ fromthose of group I1 not by their branching orde rs, bu t rather by statements on homology.According to these statements, all characters have a unique origin in the hypotheses ofgroup 11, whereas in those of group I, one character must have originated twice. Asphylogenetic systematics focusses o n both holo phy ly of species sets and branching ord ers,all hypotheses presented in Figure 4 require equal at tentio n. It should be noted that thischaracter pattern is com mo nly included in mo re ample ones.If a non-encaptic character pattern can be explained most parsimoniously by variousconflicting hypotheses of relationships belong ing to gr oup I and group 11, will the y alwaysdisplay the same branching o rde rs? The answer is negative, as can be inferred fro m Figu re5, in which three potentially h om olo go us characters 1, 2 , and 3 a re affiliated to the speciessets AB, B CD , and DE , respectively. This pattern can be explained m ost parsim onio uslyby fifteen conflicting hypotheses of genealogical relationships. Four of them belong togroup I, eleven to group 11. Th e fifteen hyp otheses deal with fo urteen branching ord ers;only hypotheses I a and I Id display the same branching order. Th e method used to f indthe fifteen hyp otheses will be described in the next section.One difference between hypotheses of groups I and I1 is especially remarkab le: Allhypotheses of group I1 display mo re coherence between the species sets A, B, C , . . thanthose of group I. Graphically, the coheren ce is marked by ho rizo nta l bars in Figures 1-5.In Figure 5, only two of these bars are present in each hypothesis of group I, whereasthose of grou p I1 have fou r to ten ba rs; that is, the hypoth eses of group I have on ly 20 % ofthe maximal coh eren ce available in a hypothesis of gr oup 11. For a distinct graphical pr e-sentation of the hypotheses of Figure 5 see LOR ENZENnd SIEG (1991) (it also r esem blesthat of Fig. 6).If, additionally, character pattern s are com plete ly resolved (i. e. if all known specieshave been foun d in wh ich the characters studied are present), at least som e or even all ofthe species sets grouped by the n odes of the diagram s may be holoph yletic: I n Figures 1aand d , every species set gro up ed by a nod e is holoph yletic, wh ereas in Figure 1 b, sets Aand B, an d in Figure 1 c, set B are non-ho lophyletic. Correspo ndingly, if the pat terns ofcharacters and their states of Figures 2-5 are completely resolved, the resulting diagramscontain a mixture of holoph yletic and non-holop hyletic species sets.Polytomies as well as the mixture of holophyletic and non-holophyletic species setswithin a most parsimonious diagrams of relationships indicate that the principle of par-simony allows achievement of many diagrams which d o no t meet a ll of H E N N I G Sequire-ments of a phylogenetic system .In transfo rmed cladistic literature, problem s dealing with m or e than three species setsare often reduced of series of so-called three-taxon -problem s. In this way, a +ta xo n-problem may be reduced to four , a 5- taxon-problem to ten, and a n- taxon -problem

3-taxon-problems. This reductionistic at t i tu de of spli tt ing n-taxon-problems (n > 3) intoseries of 3-taxon-problems is misleading, as the latter can hardly deal adequately withboth branching orders and combinations of holophyletic and non -holo phy letic speciessets like th e hypo theses of Figure 5.


10/20

ABCDE

I

.

.

-

-

-

A

~

C

D

E

m30

111l1 y

3Jg 20

@30

y1


11/20

30

2

1

3

11110 y2030

whsouo

fg

F

Tsne

ccmpeeyeovcaepencbeanmopmooyb1ccn

hh

og

oceaohp4ohmboogo

togo1Noehoyhpg

aa11c

cndnhbanodh8banodaescydcomoI1abdeh

whe7oh

inupyomieadI1c,gTogoaysc

svorreeneoohccnhh


12/20

12 S. LorenzenThe permutation method of searching for all most parsimonious hypothesesof genealogical relationships explaining a g iven character patternIf any ev olu tion ary event refers either to one or igin o r to on e loss of a character, it wouldbe extremely useful to have a reliable and time-saving m eth od fo r finding all conflicting,equally most parsimonious hypothesis of genealogical relationships explaining a givencharacter pattern, regardless of whe ther these trees are bi- o r multifurcating. U nfor tu-nately, suc h meth od s cur ren tly available as com pu ter pro gra ms are still deficient in thisrespect (LORE NZ ENnd SIEG1991 ;L O RE N Z E N992).If a character pattern allows discrimination of n d ifferently cha racterized species sets,one could t ry to test all possible trees containing these species sets as terminal taxa. Thenumber of these trees, however, is trem end ou sly high (FEL SENS TEIN978): If on ly n = 10,about 2.8 x lo8bi- and multifurcating trees wou ld be possible.The hypotheses of Figure 5 have been foun d by a me th od w hich will be referred to astheperm utation method. It regards onl y characters and n ot the ir states. I t is highly effectiveand com prises the following steps:

I . Within a pattern of potentially hom ologous characters , tho se mus t be sought whichare encaptically arr ang ed relative to all othe r characters s tudie d. As has been show n, suchexclusively e ncaptic character pattern can be explained by exactly on e mo st parsimoniou shypothesis of relationships. Regardless of the non-encapsis caused by the remaining char-acters, this basic tree will be unchanged in all rival trees explaining the entire characterpattern. The refore , the furth er analysis may b e restricted to the remaining characters ar-ranged non-encaptically.2. Even w ithin the lat ter characters , so me m ay be arranged encaptically with othersand non-encapt ical ly wi th the remaining. The maximum number of such encapticallycharacters mus t be sought. Again, this encaptic patter n can be explained by a single m ostparsimonious hypothesis of relationships. T h e charac ters still left over can be rath er easilyintegrated in this hypothesis by assuming an appro priate minim um n um ber of s teps foreach of them. Fro m the hypothes is thus achieved, the minim um n um ber of steps may beinferred which is com pu lsor y for all rival, equally most p ars im on iou s hypoth eses explain-ing this character pattern.3. With out changing the minimum sum of steps, the lat ter m ay be differently attri-buted to the characters. For example, two steps may be attrib uted to character 1 and one

to character 2, o r reversely, on e step to character 1 and two to character 2 ; if tw o steps areat t r ibuted to one character, they may refer to ei ther two independent or igins o r to oneorigin and on e loss. For each character, the max imu m nu mb er of steps cann ot exceed thenumber of species sets (like A , B, C , . . in Fig. 5 ) in which it occurs. Keeping these twopoints in min d, a tableof per mu tatio ns displaying all theoretical possibilities of attributingsteps to characters must be prepared. There is no simple algorithm for doing this , butnevertheless these permutation s m ay be fou nd rat her easily. In Figures 1, 2 , 5 , and 5, theperm utation s are displayed at the roo t of each diagram. N ot e that in the case of mo re thantw o assumed steps, say three, they may refer either to three independen t or igins or to tw oindependent origins and on e loss or to one origin an d tw o ind epen den t losses. In th e caseof even furth er s teps, these may refer to primar y origin, prim ary loss, secondary origin,secondary loss, etc. As long as the principle of parsimony is exclusively applied, evenhighly subtle cases must be regarded.

4. Each pe rmu tation requires an examination whe ther it allows inferring no, one, o rseveral hypoth eses o r relationships fr om the non-encap tic character pattern. In Figure 5 ,hypotheses IIa and b refer to the same permutation, whereas those perm utation s no t al-lowing any hypothesis are depicted at the bot tom right.5. Each of these most parsimonious hypotheses must b e integrated into the single mo stparsimonious hypothesis of relationships inferred fro m th e exclusively encaptic character


13/20

Parsimony, outgr oup analysis, and theory of evolution in phylogenetic systematics 13pattern (see po int 1). In this way, all o r nearly all m os t parsi mo nio us hypotheses explain-ing th e entire original character pa ttern can be achieved.T he method described can be applied regardless of whe ther the character patterns areresolved completely or incompletely. It cannot guarantee discernm ent of every most par-simonious hypothesis of relationships explaining a non-encaptic character pattern, butrather it prevents one from overlooking certain unexpected hyp otheses. It proved to be anexcellent tool no t only in finding all most parsimonious hypoth eses of Figure 5 , bu t alsoin analysing the m olecular characters of species of Tisbe (Harp actico ida) as achieved bySTEINBRUCKt al. (1991). It seems that the per mu tatio n met ho d w ork s at least as efficientas the algorithms employed by com pute r programs designed fo r inferring all most par-simonious hypotheses of relationships from given character patterns (see LORENZENndSIEG1991).The instruction of selecting the maximum number of characters encaptic with eachoth er (see points 1 and 2 ) resembles the so-called un ique ly evolved character con cept ofLEQUESNE1975). As the latter con cep t requires neglection of the remaining characters ofthe pattern, it is not acceptable in phylogenetic systematics.It should be added that the permutation method may not o nly sup po rt phylogenetic-systematic analyses, but may even provide help in constr ucting mo st parsim onio us deter-mination keys.

The outgroup analysis-useful or useless?If only one most parsimonious hypothe sis of relationships m ay be inferred fro m a particu-lar patter n of characters and character states, it must be accepted by both prop onen ts andopponent s of the theory of evolution. In this case, the outgr ou p me tho d is no t needed forany furt her analysis.As soon, however, as any pattern of characters and c haracter states may be explainedby various rival, equally most parsimonious hypotheses of relationships, could the actu-ally so po pu lar ou tg ro up analysis (i. e. the application of the outgroup compar i sonmethod, as recommended by WATROUSnd WH E E L E R981, W IL EY 981; MADDISONt al.1984; AX 1984, 1987, 1988; RI D LE Y 986, and o th er s) be of any help in rejecting any ofthese hypotheses an d accepting the remaining as worth y of fur the r s tudy?An inspection of many papers making use of outg roup comparison has yie lded theunexpected existence of tw o basic types of that method. On e of them is fou nd to deal withincompletely resolved patterns of characters and character s tates, the other with com-pletely resolved ones. The first type will be referred to as the par sim ony analysis based ontest samples, the second as the cladistic type of outgroup analysis . A combinat ion of bothtypes is possible.A close examination of bo th types has yielded the disa ppo inting result that their appli-cation cann ot provide any result going beyond those achieved by apply ing the principle ofparsimony. Even worse, th e cladistic type of outgroup analysis may be misleading incertain cases. In th e following sections, both types of outgroup analysis will be describedand discussed separately.

O u tg ro u p ana lys i s which is ident ica l wi th a pa rs imon y ana lys isbased on tes t samplesFrequently, presence and absence of certain characters and their s tates are predom inantlyknown from species of a taxon under focus ra ther than from the whole of all knownspecies. In order to infer at least some preliminary mo st parsim onio us hypothesis of re-lationships from such p atte rn, som e furthe r species sets closely related to the taxon unde rfocus are used as test samples (usually referred to as outgro ups) for estimating th e extent


14/20

14 S. Lorenzencharac- I n g r o u p taxaters A B C D E

OutgroupsO Q 7pL(j* P

IPlPV9PFi 6 Any ou tgrou p analysis of incompletely resolved patterns of characters and their s tates isreferred to as parsimony analysis based on test samples (th e l a t t e r are usually referred to as out-grou s). In the case presented , all a-states ofcharacters 1-9 (pattern stippled) are arranged enca p-tical&, whereas the states of character s 2-11 (pattern not stippled) are arranged non-encapti-cally. According to t1: unique m ost parsimo nious explanation available in the case presented, t h ea-states of characters 2-9 must be s y n a omorphous relative to t h e correspondin states,whereas the latter must be sym plesiomor t o u s relative to the form er. States a and p ofc t i rac te r1 are encaptic within both patterns; therefore, the parsimony analysis cannot yield arguments asto whether state a is apom orphou s relative to state p or vice versato w hich th e charac ters and charac ter s ta tes s tudied m ay oc cur outs ide the taxon und erfocus as well (the latter is usually referred to as the ingroup).If all character states foun d exclusively within the in gro up have an encaptic arrange-men t , w hereas the a l te rna tive s ta tes fo und w i th in both t he ing roup and ou tg roups a rearranged non-encaptically, only one most parsimonious hypothesis of relationships canbe inferred from this pattern (for an example see the states of characters 2-9 in Fig. 6 ) .Such hypothesis wo uld inc lude the fo l lowing s ta tements:- T h e n u m b e r of steps assumed m us t be exactly equal to t he number of character statesconsidered, as any oth er hypothesis would require the assumpt ion of mo re s teps.- Because of their assumed unique origin, a l l character states mus t be homologies of theircorr esp on din g species sets.- All encaptically arranged homologous character states (a-states of characters 2-9 inFig. 6) m us t be primarily absent outside of their corre spo ndi ng species sets, whereas allnon-encaptically arranged hom ologous character states (p-states of characters 2-9) m u s t

be secondarily absent outside of the i r corresponding spec ies se ts . Therefore , wi threspec t to the spec ies se ts considered, th e form er homologies const i tu te synap om or-phies relative to the lat ter homologies and , vice versa, the lat ter homologies con sti tu tesymplesiom orphies relative to the former.- As th e pa t t e rn of character states in incompletely resolved, it doe s not al low inferenceof any hypo thes i s on the ho lophy ly of any species set considered.If the character states are arranged less favourably withi n the in gro up and o utgr oup s, i . e .

if even th e character states foun d exclusively within the ing rou p are non-encaptically ar-ranged o r if all character states are arrang ed encaptically (as in Fig. 3), the parsimony ana ly-sis outl ined n o longer permits inference of any uniq ue hypothesis of re la tionships , hom ol-ogy, synapormorphy , o r symples iom orphy f rom th is pa tt e rn .Apparent ly , NELSONn d PLATNICK (1981: 38) an d FARRIS1982: 329) referred to t h eparsimony ana lysis based o n test samples whe n they s ta ted tha t Ou tgr ou p comparison iseven mo re o bviously an application of t he pa r s imony c r i t e r ion .


15/20

Parsimony, outgroup analysis, and th eory of evolution in phylogenetic systematics 15

Cladis t ic type of ou t g r ou p a na lysi s - useless, ev en m isleadin gIn contrast to th e firs t type of ou tgro up analysis , the par simo ny analysis based o n testsamples, the cladistic type of outgroup analysis can only be applied after having madecertain assumptions on the h olop hyly of selected species sets. As such assu mp tion s canonly be inferred from com pletely resolved patterns of characters and charac ter states, thecladistic typ e of ou tg ro up a nalysis is restricted to the analysis of these pat terns . A s long asonly the principle of parsimony analysis and the outgroup comparison method are ac-cepted as analytical tools in phylogenetic systematics, assumptions on the holophyly ofspecies sets can only be obtained by a parsimony analysis. According to Ax (1988: 76,translated from the G erm an text), th e assumptions to be made are the following:

- At least 3 real unities of nature - evolutionary species or closed communities ofdescent - compose the ingro up. Together, the 3 unities must be sho wn o r at least sup pose dto be rnon ophyletic (i. e. holop hyletic).- Within this supraspecific ingroup, at least one character must occur in alternativestates.

- O n e of these alternative states mu st occur in the so-called ou tg ro up as well whic h iscomp osed of species related to the ingroup.Th e alternative states of a character are allowed to refer to- presence and absence of a character or to- two states of a character.If the prerequisites mention ed are fulfilled, the cladistic type of out gro up analysis is saidto allow conc lusions of the following sort:If a feature occurs as alternatives in a supposed ly mo no ph yle tic gr ou p of spec ies (i. e.in the ingroup), than that feature state which also occurs outside the group (i. e. in theoutgroup) is probably the plesiomorphy. (Ax 1987: 115; 1988: 76). Consequent ly, thefeature state exclusively present in the ingroup is probably apomorphous relative to itsalternative state present in b oth the in- and ou tgrou p.In or der to evaluate the ou tgro up com parison metho d as described by AX and , s imi-larly, by W ILE Y1981), two cases shall be distingu ished:Case I (only presence and absence of a character are considered ).1 . If a completely resolved character pattern is entirely encaptic, each no de of the resultingdiagram of relationships gro up s together a holoph yletic set of species. Therefore , the pre-requisites for applyin g the cladistic type of outg roup analysis are fully satisfied. Th e lat terwill demo nstrate u nequivocally, that each of these characters consti tutes a sy nap om orp hyof its corresp onding species set relative to its primary absence elsewhere. As the resultsachieved by both the parsimony and the outgroup analysis coincide completely in thiscase, the ou tgr ou p analysis is not n eeded.

2 . If, however, a completely resolved character pattern happens to be non-encaptic,in- and outg roup s canno t be chosen unambiguously. In Figure 5, for example, hypoth esisII a wou ld a llow taking AB C as a supposedly holophyletic ingroup , whereas hypo thes isI1 b would a llow such supposi t ion for C D E ; hese supposit ions co ntradic t each other . Thechoice of ou tgr ou ps is no less ambigu ous. Fo r example, hypothesis I1 a of Figure 5 wouldallow to take D, E, o r DE as outg roup s of A B C ; if D is chosen, 2 would be secondarilyabsent in A; if E is chosen, 2 wou ld be primarily absent in A ; i f DE is chosen, a clear-cutinterpretation would be impossible. A s there i s no a lgori thm for choos ing the r ig ht in-and ou tgrou ps, the cladistic ty pe of ou tgro up analysis c anno t prov ide any help in selectingamong various, equally mos t parsimonious hyp otheses of relationships.3. If a non-en captic, com pletely resolved character pattern ca n be explained by asinglemost parsimonious hypothesis of relationships, the prerequisites for ap plyin g the cladistictype of outgroup analysis are fully satisfied. Figure 2 refers to such examples. If, in


16/20

16 S. LorenzenFigure 2c, ABC is taken as a holophylet ic ingroup and D as i ts outgroup, character 1wou ld be secondarily absent in C. If, instead, F is taken as an ou tg ro up to AB C, character1 would be primari ly absent in C. T h a t is, the cladistic type of outgroup analysis - fperform ed at all - could suggest hypotheses contradicting th ose achieved by applying theprinciple of parsimony alone (according to which 1 must be secondarily absent in C).Therefore, the cladistic typ e of out gro up analysis is not on ly useless, bu t even misleadingin this instance.Case I I (in addition to presence an d absence, different states of a character are considered).As s oo n as different states of a character are included in a phylogenetic-systematic analysis,subst i tu t ion of prior b y s ubseq uent character states may occur. In these cases, neither en-captic nor non-encaptic patterns of character states may al low unam biguo us determin a-tions of in- an d outg roup s. Fo r an example consider Figure 3, in which both the charactersand their states are arranged encaptically: According to the hypotheses a, c, d, e, andh, A B could be a holophylet ic ingro up and C i ts outgr oup , w hereas according to hypo-thesis g, BC could be a holophylet ic ingroup and A i ts outgroup. These assumptionscontrad ict each other. Again, there is no algorithm for choosing the right in- and out-groups.To su mm arize: Whenever the cladistic typ e of o utgr oup analysis can be applied unam-biguously, it is no t needed, an d whenever it is needed, it can not be applied unambiguously.Regardless of whe ther an o utg rou p analysis refers to a parsimony analysis based on testsamples or to the cladistic type, it is completely useless fo r rejecting even o ne of various,equally most parsimonious hypotheses of relationships inferred from any particularpattern of characters and character states.

The theory of evolution as an essential analytical tool in phylogeneticsystematicsT he essential part of Darwins th eory of evolution is the theor y of natural selection. Essen-tially, the latter th eory still remains valid. It has been successfully applied no t only fo rexplaining various evolutionary processes, but for explaining many kinds of organic andinorganic self-organization as well (for argum ents see Lorenzen 1989).A s the theory ofnatural selection is also essential for substantiating the thebry of descent , the union ofbo th in to t he t heory of evolu tion is justified.Regardless of proposals for modifying the theory of natural selection, the followingaspects of th e theo ry are generally accepted:1. In all species, population growth is dominated by non-linear laws caused by theability of populations to gr ow expo nentially as well as by the dens i ty dependent inhibi t ionof this grow th.2. As differences of fitness occu r within all species, struggle fo r life may brin g mo resuccess to the fittest than to the lesser f i t com peti tors. Th e fitness of an organism is deter-mined by properties of bot h the organism and its enviro nm ent.

3 . Orga nism s with n ew structures and, hence, with n ew characters always originateby variation of some existing material basis un derlyin g the develop men tof organisms char-acterized by an ancestral set of structures.4 . As soon as the origin of new structures and/or the reduction of ancestral onesprovide organisms w ith advantages in comp eting for traditional resources o r in exploitingnew one s, the n ew features may accum ulate within a species o r may even give rise to newspecies.In phylogenetic systematics, the the ory of evolut ion m ay be employed in the fol lowingway:


17/20

Parsimony, outgroup analysis, and theory of evolution in phylogenetic systematics 17As lon g as a character pattern m ay be explained by a single most parsimonious hypo-thesis of relationships, characters and character states must be h omolog ized and polarizedas indicated by this hypothesis. Th at is, the th eor y of evolut ion can only be used f or con-

firming the results achieved by applying the principle of parsimony: Evolution must beassumed to have occurred as indicated by the respective hypothesis.As soon, however, as a character pattern may be explained most parsimoniously byvarious rival hypotheses or relationships, the theory of evolution and its implicationsprovide t he o nly available analytical tools for rejecting so m e or, at best, all but one ofthese hypotheses. An example (see Fig. 4a ) shall dem ons trate this typ e of analysis:In Pterygota, the characters pterygote wings present and holometabo ly present are ar-ranged non-encaptically : Winged Hem imeta bola have wings but no holometaboly,Siphonaptera (flees) have holometaboly but no wings, whereas winged Holometabolyhave wings as well as holometaboly. A s bo th characters refer to highly complex structures ,it is mo re probable that bo th have evolved only o nce in evolution rather than on e of themhaving evolved once and the othe r at least twice. Therefore, hypotheses Ia and I b mu st berejected, whereas hypothese IIa and I1 b require further analysis. As various pterygotetaxa contain bo th winged and w ingless species and as the latter are generally adapted tocertain life styles such as ectoparasitism o r life o n w ind y islands each favouring wingless-ness, a nd as there is not th e slightest evidence that holom etab oly m ight be reduced in anyspecies of the Hemimetabola, i t is mor e probable that- wings are secondarily absent in flees, and holometaboly is primari ly absent in Hem i-metabola, than that- wings are primarily absent in flees, and holometaboly is secondarily absent in Hemi-metabola.That is, hypothesis IIa m ust be rejected, whereas hypothesis I I b mu st be accepted.Although the arguments used are familiar, it seems that the wh ole context in whichthey are used is less so. Generally, if argum ents are presented substantiating the view ofthe unique origin of all characters dealt with, those am ong conflicting mos t parsimonioushypotheses of relationships mu st be selected for furth er analysis which are provided w iththe highest homolo gy index H L . T his index was introduced and discussed by LORENZEN(1992). It has been defined as follows: H L = No. ofi nte ger characters analysed divided byNo. ofas sume d origins of these characters. In Fig. 4, H L = 2 /3 = 0.67 in hypotheses I a and b,and H L = 2 / 2 = 1.0 in I1 a and b. In Fig. 4, which deals with characters and its states,H L = 215 = 0.4 in hypothesis a, H L = 2 / 4 = 0.5 in hypotheses b and c, and H L = 2 / 2 = 1.0in hypotheses d-h. In Fig. 5 , H L = 3/5 = 0.6 in hypotheses Ia-d, H L = 3 /4 = 0.75 inIIa, b, d-i, and H L = 3 / 3 = 1.0 in IIc, j , k.Th e examples of Figures 3-5 clearly dem on-strate the imp ortance of substantiated hypotheses of homology to the process of selectingamong equally parsimonious hypotheses of relationships inferred from a particularpattern of characters and their statesIn many cases, reduction of structure s may occur in successive steps, whe reby ad-vanced stages of reduction are called vestiges ( R u d i m e n t e in G erm an) . In these cases, thetheo ry of natural selection may be employed by sho win g that vestiges are -in a phylogene-t ic sense - disappearing rather than originating structures. In this way, a sequence of char-acter states may be polarized.Even if one origin and on e loss of a complicated character is accepted as m ore pro bab lethan the double origin of such character (2 steps in each case), the theory of evolutionprovides t he only justification of tha t choice.Three aspects concerning each use of the theory of evolution in phylogenetic systema-tics sho uld be stressed:

1. Th e theo ry of evolution is not used for analysing characters and their states indepen-dently from each other but rather for analysing conflicting, equally most hypotheses ofrelationships inferred from patterns includ ing these characters and their states.


18/20

18 S. Lorenzen2. Basically, estimations o n the unique o r multiple origin of characters serve for s ub-stantiating hypotheses o n the hom olog y of characters and their states, whereas estimationson the adaptive importance of structures and their modificat ions to the respective or-

ganisms serve for substantiating hypotheses o n the polarization of sequences of charactersstates.3 . In the vein of substantiating hypotheses of relationships, each primary and secon-dary absence of characters and character states may b e regarded as different homologies ofthe co rres pon din g species sets. For example, winglessness ma y be regarded as a hom olog yof the so-called Apterygota and as a different homology of the flees. The concept ofho mo log y m ay be applied in these cases, as homologies (in a phylogenetic sense) are no tsubstantiated by applying th e so-called main criteria of homology, but rather by applyingbot h th e principle of parsimony an d the theory of evolution.

DiscussionIn this paper, thr ee analytical tools used in systematics have been analysed: the principleof parsimony, the outg roup compar ison m ethod, and the theory of evolution. It has beenshown that the f irst and the third of these tools are highly important, whereas the out-group comparison method is completely useless in systematics. Especially, the employ-me n t of the theory of evolution m akes phylogenetic systematics su perior to any kind ofaphylogenetic systematics, transformed cladistics included, as no aphylogenetic methodis available for selecting amo ng conflicting, equ ally mo st parsimoniou s hypotheses of re -lationships inferred from a particular pattern of characters and character states.Ho we ver im por tant the principle of parsimony m ay be in systematics, there will alwaysbe some difficulty as to whe the r t he min imum num ber of changes within a pattern ofcharacters and their states must be coun ted or instead the m inimu m nu mb er of evolutio-nary events having caused these changes. The se numb ers d o no t need t o be identical. Th eco m m on pract ice of coun ting exclusively the n um ber of changes mentioned is coveredneither b y the principle of parsimony nor by the theory of evolution. Despite of this diffi-culty, the principle of parsimony may at least be useful for avoiding apparently super-fluous assumptions when trying to explain a pattern of characters and their states mostparsimoniously.Although the outgroup comparison method is completely useless, i t is still ratherpopular . The only answer I can provide for explaining this paradox is the following:Ne ither in phylogenetic systematics nor in tran sfo rm ed cladistics has the impo rtance beenstressed of seeking all know n species characterized b y characters and their states studied.This m ight provide the reason w hy the two types of outg rou p analysis termed parsim onyanalysis based o n test samples an d cladistic typ e of outg rou p analysis have not beenrecognized and , hence, seem to have been confused.It s hould be stressed that even the employment of both the principle of parsimony andthe theory of evolution cannot guarantee finding the definite phylogenetic system of allorganisms. Therefore, phylogenetic systematicists should point u nam biguo usly to insuf-ficiencies of their results achieved and resist th e tem pta tion of excluding difficult charac-ters and character states or difficult species from an phylogenetic-systematic analysis o rof employing arbitrary algorithms (like those offered by phenetics) for achieving resultseven in difficult cases. Such results wo uld o nly pro vide pseudo solutions to phylogene-tic-systematic problem s.W ith respect to approximating a (not : the ) general reference sys tem (HENNIG966),phylogenetic systematics based on both the principle of parsimony and the theory ofevolution is super ior to any kind of aphylogenetic systematics.


19/20

Parsimony, outgr oup analysis, and theory of evolution in phylogen etic systematics 19Acknowledgement

I would l ike to than k PATRICK IN G LE , iel , for a linguistic revision of the text.Zusammenfassung

Die Bedeutung der Sparsamkeit, des Au~engruppenvergleichsund der Evolutionstheorie in derphylogenetischen SysternatikIn einer detaillierten Analyse wird gezeigt, dafl sow ohl das Prin zip d er Sparsamkeit als auch dieEvolutionstheorie - peziell die Selektionstheorie - unverzichtbare analyt ische Werkzeuge in d erphylogenetischen Systematik darstellen, wah rend der heutzutag e so populare Auflengruppenver-gleich nu tzlo s und gelegentlich sogar irrefiihrend ist.Es werden zwei Typen von M erkm alsm ustern unters chiede n: vollstan dig und unvollstandigaufgeloste . In ers teren s ind fur a lle untersuchten Merkm ale und Merkm alsauspragungen jewei lsalle beka nnten A rten e rmitte lt wo rden, bei denen sie vor kom me n, in letzteren ist dies nicht derFall.Je nach Struk tur e ines Merkm alsmusters kann es durch e ine e inzi e oder durc h verschiedene,gleichermaflen sparsamste Verwandtschaftshypothesen rk la r t wer ten . Die S t ruk tu ren d iese rMerkm alsmuster werden e ingehend analysier t. Es wird die sogen annte Perm utat ionsmethodeein efiihrt , die die Suche nach konkurrierenden sparsamsten Verwandtschaftshypothesen er-leicttert .Die Niitzlichkeit des Prinzips der Sparsamkeit wird ein eschrankt durch die Unsicherheit ,ob entweder die Mindestzahl von Veranderungen innerhafb e ines Merkmalsmusters gezahl twerden sol1 ode r aber die Mind estzah l von evolutionaren Ereig nissen , die diese Veranderungenbewirkten. O bw oh l beide Zahlen verschieden sein konne n, wird aus Gri ind en der Einfachhei tgewohnlich die erste bevorz ugt.Es w urd e gefun den, dafl vom Auflen ruppenvergleich zwei Type n existieren, die als Sparsam-keitsanalyse nach dem Stich ro be nv er ih re n und als kladis tischer Typ des Auflengruppenver-e ichs bezeichnet w erden. i e i d e Typen s ind voll ig ungeei net , auch n ur e ine von m ehrerenfon kur riere nde n, gleichermaflen sparsamsten Verwandtschafishypo thesen zur i ickzuweisen .Nach heutiger Kenntnis ist dies allein durch A nw end ung der Ev olution stheor ie (die die Selek-tionsth eorie einschlieflt) moglich. Jedoch konn en auch dann nicht alle phylogenet isch-systemat i -schen Prob lem e gelost werden.Insgesamt erweist sich die phylogenetische S ystem atik trotz aller U nzulan glichk eiten jederForm aphylogenet ischer S s temat ik (zu er auch die t ransformier te K ladis t ik gehort ) als iiberle-gen beim Versuch, ein (n ic tt : das) , ,allgemeines Bezugssystem" de r Lebe wes en zu erarbeiten .

ReferencesAx, P., 1984: Das Phylogenetische System. Syste ma tisierung der l ebenden Na tu r au fg rund ih rerPhylo enese . Stut tgar t : G . Fischer .- 1987: %he p hylog enetic system The sys tem atization of org anism s on the basis of theirphylogenesis. Chichester, N ew York: J . Wiley.- 1988: Systernat ik in der Biologie. D ars te l lung der s tam mesgeschicht l ichen Or dn un g in derlebenden Natur. Stuttga rt: G . Fischer.BEATTY,., 1982: Classes and cladists. Sy st. Zo ol. 31, 25-34.B O C K ,W. J., 1981: Func tional-a daptiv e analysis in evolu tionary classification. Amer. Z ool. 21,B O C K ,W. J . ; V O N WAHL E R T , . , 1965: Adapt ion and the form -funct ion -com plex. Evolut ion 19 ,B R A D Y ,. H., 1985: O n the indepe nden ce of systematics. Cla distics 1, 113-126.C A R T M I L L , ., 1981: Hy poth esis testing and phylogenetic rec ons truc tion . Z. zool . Syst . Evolu-t ion.- forsch. 19 , 73-96.C H A R I G , . J . , 1982: Systematics in biology: a funda me ntal com arison of som e major scho olsof though t . In : Problems of phylogenet ic r econs t ruc t ion . Ed . gy K. A. JO Y SE Y ;A .. FRIDAY.Lo ndo n, N ew York: Academic Press. pp. 363-440.E L D R E D G E , . ; C R AC R AF T ,. , 1980: Phylogenetic patterns and the evolutionary process.Method and theo ry in comparat ive biology. N ew York: Colu mbia Univers i ty Press .F A R R I S ,. S., 1982: O u t roup and parsimony. Sy st . Zool . 31, 328-334.FELSENSTEIN,. , 1978: l%e num ber of evolu tionar trees. Syst. Zo ol. 27, 27-33.H E N N IG , ., 1949: Zur K larung e iniger Begri fL der phylogenet ischen Systemat ik . Forsch.-

5-20.269-299.

Fortschr. 25 , 136-138.1966: Phylo genetic systematics. Urb ana, Chica go: University of Il l inois Pre ss.


20/20

20 S.LorenzenL O R E N Z E N ,. , 1989: Evolu tion im Spannungsfeld zw ischen linearer und n ichtlinea rer Wissen-schaft. Universitas 1211989, 1149-1159.L O R E N Z E N ,. ; SIEG, . , 1991: P H Y LI P, P A U P an d H E N N I G 8 6 - how reliable are these co m -puter program packages used in systemat ics? Z. 2001. Syst . Evolut . - forsch. 29, 466-472.L O R E N Z E N ,. , 1992 : PHYLIP , PA UP and H E N N I G 86 need improvement . In t roduc t ion of thehom ology index. Z. zool. Syst. Ev olut.-fors ch. 30, 249-255.M A D D I S O N , . P.; D O N O G H U E , . J . ; M A D D I S O N , . R., 1984: Outgroup analysis and par-simony. Syst. Zool. 33, 83-103.MA YR, ., 1969: Principles of sys tem atic zoology. Ne w York : McGraw-Hi l l . (deu t sch : Grund la -gen de r zoologischen System at ik . Ber lin , H am bu r :Paul Parey 1975.)NAEF,A. , 1926 : Zur Diskuss ion des Homo log iebegr iks und se ine r Anw endung in de r Morp ho-logie. Biol. Ztr1.-blatt 46, 405-427.NE L S O N, . J . ; P L AT NIC K, . , 1981 : Systematics and biogeography. Cladistics an d vicariance.N ew York: Colu mb ia Univ. Press .PATTERSON, . , 1980: Cladistics. Pattern versus process in na ture : a personal view of a methodan d a controversy. Biologist 27, 234-240.PETERS, . S . , 1976: Evolut ion stheor ieu nd S s temat ik . J . O r n . 117, 329-344.PETERS,D. S . ; G U T M A N N ,. F., 1971:Ub e r i e e s ri c ht u n g v on Me rk mal s- u n d Ko n s t r u k ti o n s -re ihen. Z. zool. Syst. Evolut.-forsch. 9, 237-263.P L AT NI C K,. I. , 1980: Philos ophy and the tra nsfo rm atio n of cladistics. Syst. 2001.28, 537-546.L E Q U E S N E , . J . , 1975: Th e u niquely evolved character concep t and i ts c ladis t ic appl icat ion.R E M A N E ,., 1956: Die Grun dlagen des natiirl ichen System s und der Phylo genetik . Theo retischeRID LEY , . , 1986: Ev oL tio n and c lass i fication. Th e reformat ion of c ladism. L on don , New York:SCHMITT.M.. 1985: Thesen zu r Theorie und Me thodo loeie der Phvloeenet ischen Svsternatik .

Syst. ZOOI.23, 513-517.Morphologie und S stem atik. Leip zig: Ak ad. Verlagsgesellschaft Gee s & Port ig .Longman .

" I UZool..Beitr. N. F. 29, 19-23.SLU YS. . . 1988: O n adaptat ion, th e assessment of adaot ions . and the value of adaotive areu-ments in phylogenetic ' reconstruct ion. Z. zool. Syst . Evolut . - forsch. 26 , 12-26.SNEATH, . A . ; SOK AL , . R. , 1973: Num erical taxonomy. The principles and pract ice of nume r-ical classification. San Francisco: Freem an.S T E I NB R UC K,. ; S C HL E GE L , . ; K R A M E R , . ; K U P F E R M A N N ,., 1991: Ident i f ica t ion andphylogenetic analysis of four Tisbe s ec ies (Crustacea , Copepoda) us ing D N A res tr i c tionsite variation. Z. 2001. S ys t. E v o l u t . - i r s c h . 29, 393-408.SZALAY,. S.; B O C K ,W. J., 1991: Evolutionary theory and systematics: relationships betweenprocess and pat terns . 2. zool. Syst. Evolut.-forsch. 29, 1-39.WATROUS. . E . :W H E E L E R . .D.. 1981:Th e ou t -e rouD comoar i son m ethod of charac ter analv-

* "

0 ,sis. Syst. Zool. 30, 1-11:York, Chichester, Brisbane, Tor ont o: J . Wi L y .

'

WILEY,E . O., 1981: Phylogenetics. The theor and practice of phylogenetic system atics. N ewAuthor's address: P r iv . -Do z . Dr . S I E VE R T OR E N Z E N ,oologisches Institut der Universitat ,Olsh ausen str. 40, W-2300 Kiel, F R G

Documents

The Role of Parsimony